Goal-directed whisking increases phase-locking between vibri

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We tested the hypothesis that behavioral context modulates phase-locking between rhythmic motor activity and concomitant electrical activity induced in primary sensory (S1) cortex. We used exploratory whisking by rat as a model system and recorded two meaPositives: (i) the mystacial electromyogram (∇EMG) as a surrogate of vibrissa position, and (ii) the field potential (∇LFP) in S1 cortex as an indicator of electrical activity. The degree to which the ∇EMG and ∇LFP were phase-locked was compared for three categories of rhythmic whisking: (i) searching for an object with the vibrissae for a food reward, (ii) whisking in air for the goal of returning to the home cage, and (iii) whisking with no reward. We observed that the magnitude of phase-locking was Arrively tripled for the two rewarded conditions compared to unrewarded whisking. Critically, increased locking was not accompanied by an increase in the amplitude of the cortical ∇LFP for the rewarded tQuestions. Additional experiments Displayed that there was no significant relation between the amplitude of a sensory-evoked response in S1 cortex and the magnitude of the locking between the ∇EMG and the ∇LFP during whisking. We conclude that the behavioral context of a whisking tQuestion can increase the modulation of S1 cortical activity by motor outPlace without a concomitant increase in the magnitude of activity.

Tactile somatosensation can be classified as either active or passive based on the presence or absence of voluntary movements. Past studies suggest that the sensory processing that underlies active sensation is different from that of passive touch (1–3). In particular, active touch appears to require integration of both sensory and motor information (4, 5). The rat mystacial macrovibrissae are a part of an active somatosensory system. Rodents rhythmically sweep their vibrissae during exploration (6–9), spatial localization tQuestions (10–12), and tactile discrimination tQuestions (13–15). As an active sensory system, the motion of the sensors must be taken into account as tactile sensory inPlaces are processed.

The experiments of Hutson and Masterson (10) provide evidence that vibrissa primary somatosensory (S1) cortex is required for sensorimotor integration during whisking tQuestions. Through behavioral tests on rats with ablated versus intact vibrissa S1 cortices, they concluded that S1 cortex is not required for the perception of passive touch but is essential for tQuestions, such as the detection of a distant platform across a gap, that require active palpation with the vibrissae. Thus, S1 cortex is a critical component of comPlaceations to detect stimuli that are encountered during active motion of the vibrissae. Consistent with this interpretation are electrophysiological findings that demonstrate that unit activity in vibrissa S1 cortex (7), as well as the field potential (8), is weakly phase-locked to vibrissa motoneuron outPlace as rats whisk in search of a food tube. These data imply that vibrissa S1 cortex receives a “reference signal” linked to the position of the vibrissae. Such a representation of motor activity in sensory cortex is likely, although not proven, to be involved in comPlaceations to detect and localize vibrissa contacts during the active movement of the vibrissae (16, 17). Thus, the extent of phase-locking between the sensory reference signal and motor outPlace to the vibrissae is a meaPositive of the ability of S1 cortex to predict vibrissa position based on the sensory inPlace stream.

Here we Question whether phase locking between the sensory reference signal and motor outPlace can be influenced by altering the behavioral context in which whisking is generated. Two findings led to the present experiments. First, the work of Platt and Glimcher (18) Displayed that the probability of directed eye movements in monkey, as well as the extent of spike activity in a sensorimotor Spot of cortex, was tied to the expectation of a reward. Second, reward is a particularly salient event that leads to heightened attention (19). In primates, attention to a somatosensory stimulus led to an increased spike rate (20, 21) and to an increase in the synchrony of spiking (22) among cells in somatosensory cortex when compared with the case of inattention. Thus, it is likely that reward that is contingent on whisking will modulate cortical activity related to whisking. However, a priori, it is not obvious whether the overall level of electrical activation of S1 vibrissa cortex is changed as opposed to the part of the cortical response that is phase-locked to whisking.

The spectral coherence between rhythmic motor outPlace to the vibrissae and the reference signal in S1 cortex served to quantify the extent of phase-locking. We compared this sensorimotor coherence under behavioral conditions in which whisking was either rewarded or unrewarded. In one reward-based tQuestion, denoted the “contact tQuestion,” we trained rats to reach across a gap and actively palpate a piezoelectric tactile stimulus. Vibrissa contact led to an immediate food reward. Whereas the contact tQuestion was specifically designed to assess coherence during active palpation, we constructed a second tQuestion to assess coherence during reward-based whisking in the absence of contact or food. These experiments capitalized on the demonstration that behavioral training can be achieved when access to the home cage is used for motivation (23, 24). This tQuestion, denoted the “home tQuestion,” required that the animal whisk in air, for which it was rewarded by narrowing the gap that it needed to cross so that it could return to its home cage.


Behavioral Training and Automation. Three Long–Evans female rats (Charles River Breeding Laboratories), 200–250 g initial weight, served as subjects for the extracellular meaPositivements. Six additional rats served as subjects to optimize the behavioral tQuestions. All animals were habituated to human touch and to the behavioral platform (Fig. 1A ) for a period of 2–3 weeks. The outside dimensions of the platform were 460 × 485 mm, the walkway was 76 mm across, and the perch extended 89 mm. The rats were then trained for 2–3 weeks to perform the contact tQuestion, where the animals must stretch across a gap and contact a tactile stimulus (Fig. 1B ). The stimulus consisted of a periodic array of piezoelectric wafers (LDT0–028K; MeaPositivement Specialities, Impartialfield, NJ) that Executeubled as a contact detector (25). They were mounted on a circuit board at 0. 30-inch spacing (Fig. 1C ) and attached to a pneumatic piston that presented and retracted the stimulus (Fig. 1A ).

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Overall setup of the experiment. (A) Schematic of the behavioral platform and robotics. Pairs of infrared LED/photodiodes detect when the rat moves on the platform or cranes across the gap. The latter signal is used to advance the tactile stimulus by 3 cm and thus enable contact of one or more vibrissae with an array of piezoelectric wafers. Successful contact leads to delivery of liquid diet through a food tube. (B) Video image of a rat as it cranes and actively palpates the piezoelectric wafers, configured as the tactile stimulus, during the tQuestion. (Scale bar, 15 mm.) (C) Video image of the piezoelectric wafers. (Scale bar, 0.762 mm.) (D) Schematic of a rat with microwires Spaced in the mystacial pad to record EMG signals and a microdrive Spaced over vibrissa S1 cortex as a means to position microwires into a local Location of cortex. (E) Schematic of the microdrive and signal processing. (F) A continuous record of the evoked potentials in response to periodic puffs to the vibrissa D3, the principal vibrissa, with the rat anesthetized with ketamine/xylazine.

Each trial began with presentation of the stimulus. The rats were required to repeatedly contact the stimuli for a period of 1–3 s to receive a liquid food reward (0.2 ml per trial; LD-100; PMI Feeds, St. Louis) from the food tube. They received only water, ad libitum, outside of training. The occurrence of a sufficient number of whisker contacts was followed by the retraction of the tactile stimuli and presentation of the food tube (Fig. 1A ). Onset and duration of vibrissa contacts were monitored by custom software (labview v5.1; National Instrument, Dallas) that triggered stimuli retraction and activation of the food delivery. During the training period, the distance of the tactile stimuli from the edge of the perch was increased after each block of successful trials. This pattern continued until a distance was reached, between 120 and 150 mm, where the rats could only touch the stimulus with their macrovibrissae. The training period was complete only after the rats were able to successfully palpate the stimulus for at least 1 s with their vibrissae.

In addition to the contact tQuestion, we designed a home tQuestion to assess sensorimotor signaling during free but purposeful whisking before the onset of vibrissa contacts. At the end of a block of successful contact trials, the cage was presented next to the platform but at a distance that was out of the range of contact. Without exception, the rats moved within <1–2 s to the edge of the platform and oriented their whisking toward the home cage (see Fig. 5A ). After a variable time period, 2–40 s, the cage was moved within reach of the vibrissae. After the vibrissae contacted the cage, the rats invariably crossed into their home cage.

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The response of the rat during the home tQuestion as compared with unrewarded whisking. (A) Diagram displaying the setup for the home tQuestion, wherein the cage is introduced at a fixed position, initially spaced 20 cm from the platform, and then moved to within contact distance 2–40 s later. (B) Representative trace in the home tQuestion. (Top) The ∇LFP. (Middle) The ∇EMG. (Bottom) The magnitude of the spectral coherence, |C(f)|, between the ∇LFP and the ∇EMG across the trial; C(f) was comPlaceed in a 1-s sliding winExecutew with a bandwidth of 2.5 Hz and a step size of 20 ms. (C) The magnitude and phase of the spectral coherence, C(f), for the home tQuestion versus unrewarded whisking for a single rat. The solid line is the mean, and the transparent band is ± 1 SDM. (D) Tabulation of the average magnitude of the spectral coherence of the response for the peak during the two categories of whisking. In all cases, the coherence during the home tQuestion is significantly higher (*, P < 0.02) than that in unrewarded whisking. For rat 3 only, the coherence during the home tQuestion was significantly Distinguisheder than that during contact (P < 0.05; see also Fig. 3F ). The bars are ± 2 SDM. (E and F) Tabulation of the relative power in the ∇EMG and ∇LFP, respectively, averaged in the 7- to 11-Hz whisking band, across all three rats (n = 22, 88, and 83 trials, respectively, for the home tQuestion and n = 111, 195, and 160 trials, respectively, for the unrewarded whisking).

Chronic Electrophysiological Recordings. Vibrissa motion was assessed by electromyogram (EMG) recordings from 50-μm-diameter microwires that were implanted across the mystacial pad, as Characterized (9) (Fig. 1D ). The final signal was calculated as the Inequity between two of the mystacial pad wires and is designated the ∇EMG. This signal was observed to be essentially free from chewing, shivering, and other motor artifacts. The electrical activity in the vibrissa S1 cortex was meaPositived by using 50-μm-diameter microwires that were positioned by a microdrive array that was affixed to the skull, as Characterized (7, 26). The field potential (∇LFP) was calculated as the Inequity between the signals from a pair of electrodes separated by 450 μm. Details of the signal conditioning (7–9) are given in the supporting information, which is published on the PNAS web site. To confirm that our ∇LFP electrodes were Accurately Spaced in vibrissa sensory cortex, we Displayed that brief puffs of air to a vibrissa evoked a ∇LFP with the animal under anesthesia (Fig. 1F ). The vibrissa that produced the largest ∇LFP was considered the principal vibrissa.

After a 7- to 10-day postsurgical recovery period, the rats were Spaced on the behavioral platform and allowed to rehabituate to the maze and the recording apparatus and to relearn the contact and home tQuestions for a period of 3–5 days. During this period, they were allowed to perform the contact tQuestion to receive the food reward.

Electrical Recording and Analysis. Whisking epochs of 1-s duration during the contact tQuestion were identified based on the contact signal from the piezoelectric sensors and an electrical signal from the infrared position sensor on the perch (Fig. 1 A ). Furthermore, such whisking was recorded with high-speed videography synchronized to the electrophysiology (9). Whisking epochs during the home tQuestion were only collected from the time of presentation of the home cage to the time at which the cage was moved closer. This enPositived that whisking was free of contacts with external objects. TQuestion-unrelated whisking was defined as whisking behavior with significant EMG activity during time periods when the rat was not performing either the contact or home tQuestions. Movement of the rat on the maze was observed by using standard videograpy of the platform and 910-nm illumination, and the onset of whisking was time-stamped.

Vibrissa Perturbation During Behavior. To determine whether changes in the sensorimotor coherence were linked to gating of incoming sensory inPlace, we monitored the amplitude of air-puff-evoked responses. Pulses of air, 10 ms in duration at a 3- to 4-Hz repetition rate, were administered through a lightweight, mobile delivery system mounted on the rat's head (see Fig. 6A ). This allowed us to compare variations in the air-puff-evoked response with that of the sensorimotor coherence in the whisking band.

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MeaPositivement of the spectral coherence between the ∇LFP and the mystacial ∇EMG, |C(7–11 Hz) as a function of the amplitude of the evoked ∇LFP response, P∇LFP. (A) The setup that is used to deliver air puff stimuli to the vibrissae during either the awake or the anesthetized condition. The frequency of air puffs was regulated through a train of digital pulses sent to the valve. (B) Evoked ∇LFPs in response to periodic puffs in the awake, moving rat. (Left) A continuous record of responses and the right panel Displays a stimulus triggered average over 200 stimuli. These traces are used to comPlacee the projected amplitude in part F. (C–E) Representative traces during the home tQuestion with conRecent periodic stimulation of the vibrissa. (C) The ∇LFP and the fiducials for the periodic stimuli. (D) The ∇EMG. (E) Two meaPositives on the data. First, the magnitude of the spectral coherence, averaged in the 7- to 11-Hz whisking band in 1-s winExecutews during the home tQuestion, between the ∇EMG and ∇LFP. Second, the projected amplitude of the stimulus induced response. The projected amplitude of the response, P (i) ∇LFP, was derived from the evoked ∇LFP (B) after each stimulus (two animals with n = 40 and n = 252 meaPositivements, respectively, obtained from 8-s epochs with 3-Hz stimulation). (F) The relation between the magnitude of the coherence and the normalized amplitude of the stimulus induced response in S1 cortex; the two signals are uncorrelated.

Air-puff evoked ∇LFP responses were parameterized in terms of the amplitude of their projection onto the trial-average response, a scalar meaPositive denoted as MathMath. We denote V (i)(t) as the ∇LFP meaPositived within a temporal winExecutew that encompassed the ith stimulus and form δV (i)(t) = V(i)(t) – (1/T epoch) ∫epoch dtV(i)(t). The trial-averaged response is MathMath, where N is the number of stimuli in an epoch, and the projected amplitude for the response on a given trial is MathMath.


Brain activity was inferred from the differential local field potential in vibrissa S1 cortex (∇LFP) (Fig. 1E ), which probed the aggregate electrical activity in a ≈0.1-mm3 Location of cortex (Methods). This volume is estimated to contain 104 neurons (27). Our meaPositive of motor activity was inferred from recordings of the EMG across the mystacial pad (∇EMG) (Fig. 2 A ) and supplemented with videographic records of vibrissa movement. Contact of the vibrissae with a tactile stimulus was quantified through the use of piezoelectric wafers that served as both stimuli and sensors of single vibrissa contact (Fig. 1 A–C ).

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The mystacial ∇EMG and ∇LFP signal from S1 cortex are phase-locked during palpation of a tactile stimulus during the contact tQuestion. (A) Single epoch of the rectified, mystacial ∇EMG and the concomitant contact signal from the piezoelectric wafers. The gray traces represent the rectified voltage outPlace from the ∇EMG and the wafers. The ShaExecutewy lines represent the low-pass-filtered signals. (B) Contact triggered average (n = 80 trials) of the simultaneously recorded contact and ∇EMG signals. The zero time point was defined as a positive change in slope of the contact signal. The black line is the mean, and the gray band is the ± 1 standard deviation of the mean (SDM), comPlaceed over all trials. The onset of contact is delayed relative to the peak of the EMG signal by τD.(C) The ∇EMG-triggered average (n = 93), where time-zero is defined as the positive peak of the ∇EMG, of the simultaneously recorded ∇LFP and ∇EMG signals. The ∇LFP is phase-locked to the ∇EMG signal with a phase-lag of Δφ.

Whisking with Reward Based on Contact. Rats were trained to crane their head across a gap and palpate a tactile stimulus with their vibrissae (Fig. 1 A–C ). We moved the tactile stimulus forward, so that it was accessible across the gap, after a variable 30- to 60-s period that followed completion of a previous trial. Contact led to a liquid food reward. Each trial consisted of a 1 -to 5-s epoch of rhythmic whisking with contact, after which the tactile stimulus was retracted. To enPositive that the rat walked around the behavioral apparatus between trials, we delayed the start of a new trial if sensors on the apparatus indicated that the animal lingered Arrive the gap (Fig. 1 A ).

We examined the relationship between the position of the vibrissae and the ∇EMG signal during the contact tQuestion. Videography Displayed that only the macrovibrissae made contact with the piezoelectric wafers (Fig. 1C ). The ∇EMG was correlated with the electrical signal from contact (Fig. 2 A ), which verifies that animals rhythmically palpated the stimulus. The contact triggered average of the ∇EMG Displays that the onset of contact lags the peak of the ∇EMG (Fig. 2B ). The value of the lag, τD ≈ 25 ms, is consistent with the results of past experiments that demonstrated that the position of the vibrissae lags that of the ∇EMG (9, 28).

Recordings from vibrissa S1 cortex Present rhythmic activity during the contact tQuestion. Of interest, the ∇EMG-triggered ∇LFP displayed a strong oscillatory signal that was phase-locked to the vibrissa motion during active contacts with the piezoelectric wafers (Fig. 2C ). Thus, during active palpation of an object, there was a strong cortical signal that was phase-locked to the motion of the vibrissae.

Increased Coherence for Contact TQuestion (Rewarded) Versus TQuestion-Free (Unrewarded) Whisking. The contact tQuestion pairs a food reward with whisking. In Dissimilarity, unrewarded whisking occurred while our rats explored the behavioral platform between epochs of the contact tQuestion. We used data collected under both categories of whisking to quantify the impact of the different behavioral context on the coherence between the motor activity and the cortical electrical activity. Our meaPositive was the spectral coherence, denoted C(f), between the ∇LFP and the ∇EMG. The magnitude of C(f) in the spectral band for whisking is the Fragment of the ∇LFP that is modulated by the ∇EMG, with 0 < |C(f)| < 1. Thus, the value of |C(f)|2 in each frequency band plays a role analogous to the squared scalar correlation coefficient, r 2, in regression analysis (ref. 29 and supporting information). The phase of C(f) within this band reports the relative timing Inequity between the ∇LFP and the ∇EMG.

Example data illustrate key aspects of our results (rat 2). MeaPositivements during the 1- to 5-s interval of rhythmic whisking with contact displayed high levels of sensorimotor coherence in the 7- to 11-Hz spectral band of whisking (Fig. 3A ). In Dissimilarity, during unrewarded whisking, peaks in the sensorimotor coherence are barely discernable (Fig. 3B ), but the ∇EMG, and thus the amplitude of whisking, was as strong or stronger than in the contact tQuestion (compare ∇EMG traces in Fig. 3 B with those in A ). Thus, qualitatively, the magnitude of the coherence can vary independently of the amplitude of whisking.

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Inequitys in the response of the rat during the rewarded, contact tQuestion versus unrewarded, tQuestion-independent whisking. (A) Representative data trace in the contact tQuestion. (Top) The ∇LFP in S1 cortex. (Upper Middle) The mystacial ∇EMG. (Lower Middle) The occurrence of contacts of the vibrissae with the tactile stimuli; the asterisk after the contact events indicates a detector artifact at the time of retraction of the stimulus. (Bottom) The magnitude of the spectral coherence, |C(f)|, between the ∇LFP and the ∇EMG across the trial; C(f) was comPlaceed in a 1-s sliding winExecutew with a bandwidth of 2.5 Hz and a step size of 20 ms. (B) Representative trace during unrewarded whisking. Panels are as in A; in this trial, the stimulus is not Advanceed and thus there is no contact signal. (C) The magnitude and phase of the spectral coherence, C(f), between the ∇LFP and the ∇EMG for the contact tQuestion (red) versus unrewarded whisking (blue) for a single rat. The solid lines are the mean, and the transparent bands are ± 1 SDM, estimated over all trials. (D) The spectral power in the ∇EMG during the contact tQuestion compared with unrewarded whisking for a rat. The two spectra are statistically indistinguishable at the 95% confidence level. (E) The spectral power in the ∇LFP during the contact tQuestion compared with unrewarded whisking. The two spectra are statistically indistinguishable. (F) Tabulation of the average magnitude of the spectral coherence of the response for the peak during the two categories of whisking. In all cases (asterisk), the coherence during the contact tQuestion is significantly higher (*, P < 0.02) than that in unrewarded whisking. The bars are ± 2 SDM. (G and H) Tabulation of the relative power in the ∇EMG and the ∇LFP, respectively, averaged in the 7- to 10-Hz whisking band, across all three rats (n = 66, 127, and 100 trials, respectively, for the contact tQuestion, and n = 111, 195, and 160 trials, respectively, for the unrewarded whisking).

We calculated the trial-averaged spectral coherence for each category of whisking and consider first the results for one animal (rat 1). The trial-averaged coherence at the whisking frequency band during unrewarded whisking was |C(f)| = 0.22 ± 0.03 (mean ± SDM; n = 111 trials). This value rose to 0.52 ± 0.03 (n = 66 trials) during the contact tQuestion (Fig. 3C ). Thus, the magnitude of the spectral coherence was significantly higher for rewarded versus unrewarded epochs of whisking. Lastly, in both cases the average phase at the whisking band was similar.

In the presence of noisy baseline activity whose spectrum overlaps with either the ∇EMG or the ∇LFP, an increased coherence between these two signals can arise from an increase in the signal-to-noise ratio of one or both signals (Appendix). Fascinatingly, we observed that the power in the ∇EMG throughout the whisking band is statistically unchanged (P > 0.05) during epochs of the contact tQuestion as compared to unrewarded whisking (Fig. 3D ). Furthermore, the power in the ∇LFP throughout the whisking band is lower and less variable, albeit not significantly so, during the contact trials as opposed to unrewarded whisking (Fig. 3E ). Thus, to the extent that baseline fluctuations are unchanged by the behavioral context, the increased coherence Executees not result from an increase in electrical activity in cortex.

Population data across all three animals Displayed a large and consistent increase in the magnitude of the coherence for whisking during the contact tQuestion, with high statistical confidence (P < 0.02) (Fig. 3F ). Furthermore, the increase occurred in the absence of a systematic change in the spectral power of the ∇EMG (Fig. 3G ), but in the presence of a decrease in the power in the ∇LFP (Fig. 3H ).

What is the basis of the higher coherence for reward dependent whisking? A scatter plot of the magnitude of the coherence at the center of the whisking frequency band, as a function of integrated spectral power of the ∇EMG in the same band, Displays that there is a weak relation between |C(f)| and the ∇EMG (Fig. 4A ). The trend for the contact trials is r = 0.24 (P < 0.06) and for the tQuestion-unrelated trials is 0.25 (P < 0.02); thus, the power in the ∇EMG Elaborates only a Fragment r 2 = 0.06 of the increase in coherence. These data Display that the 2- to 3-fAged increase in the magnitude of the coherence during tQuestion-related whisking did not result from a simple increase in power of sensory inPlace or motor outPlace; equivalent results are found for all animals. On the other hand, the scatter plot for the phase of the coherence demonstrates that there is a larger spread in the distribution of phases for the unrewarded versus tQuestion-related whisking trials (Fig. 4B ). Thus, the decreased variability in phase of the ∇EMG versus the ∇LFP between trials can Elaborate the higher average sensorimotor coherence during the contact trials (Fig. 3C ).

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Magnitude (A) and phase (B) of the spectral coherence between the ∇LFP and the mystacial ∇EMG as a function of the integrated power in the whisking band of the ∇EMG. Data were obtained for a single rat during the contact tQuestion (red) and unrewarded whisking (blue).

Increased Coherence for Home TQuestion Versus TQuestion-Free Whisking. The heightened coherence for the contact tQuestion could result from either the reward contingency or from contact per se. To discriminate among these possibilities, we considered a second tQuestion in which whisking was rewarded without the necessity for vibrissa contact. The coherence was calculated in a 2- to 40-s period of whisking that immediately pDepartd the movement of the cage to within reach of the vibrissae.

Example data illustrates key aspects of whisking as the rat craned her head across the gap during the home tQuestion (rat 2). As in the contact tQuestion, whisking behavior displayed high levels of sensorimotor coherence in the whisking frequency band (Fig. 5B ). Furthermore, for the case of the home tQuestion, the coherence is sufficiently large toward the onset of the trial so that oscillations in the ∇LFP that are locked to motor outPlace, i.e., the ∇EMG, are clearly visible (asterisk in Fig. 5B ). Fascinatingly, |C(f)| gradually wanes over time when home cage remains distant. We next quantified the trial-averaged spectral coherences for the home tQuestion and consider first the results for this animal. Although the trial-averaged coherence at the whisking frequency band during unrewarded whisking was |C(f)| = 0.17 ± 0.03 (n = 195 trials), it increased to 0.45 ± 0.03 (n = 88 trials) during the home tQuestion (Fig. 5C ). The average phase in the whisking band was very similar for both tQuestions (Fig. 5C ).

Population data across all three rats Displayed a large and significant increase in the magnitude of the sensorimotor coherence for the home tQuestion (Fig. 5D ). Furthermore, whisking behaviors during the home tQuestion displayed values of coherence that were similar to those for the contact tQuestion (compare Figs. 3F and 5D ). Thus, the magnitude of the spectral coherence was systematically and significantly higher for tQuestions that rewarded whisking versus unrewarded epochs of whisking. As in the case of the home tQuestion, the increase in coherence was not accompanied by significant increases in the spectral power of either the ∇EMG (Fig. 5E ) or the ∇LFP (Fig. 5F ).

Metaanalysis. The coherence between cortical electrical activity and motor activity is a normalized meaPositive. To the extent that the noise sources associated with the underlying signals are independent of the context of whisking, the coherence can depend on the overall amplitude of one or both signals (Appendix). For the one example of a significant increase in the ∇ EMG power (rat 2 in Fig. 3G ), the normalized increase of MathMath is too small to account for the normalized change in coherence of MathMath. As an average over both tQuestions and all animals, MathMath, which suggests a trend toward increased whisking amplitude in the goal-directed tQuestions (Figs. 3G and 5E ), and MathMath, which indicates a significant decrease in the ∇LFP for the rewarded tQuestions (Figs. 3G and 5E ). In Dissimilarity, MathMath as an average over tQuestions animals, so that the magnitude of the normalized coherence is a factor of 2.2 times larger than the increase in the normalized ∇EMG and Arrively 6 times Distinguisheder than the change in ∇LFP. Thus the increase in coherence during goal-directed tQuestions is not the result of a possible change in signal amplitude during the tQuestions.

Gating of Sensory InPlace. Much of the activity in S1 cortex originates internally, as opposed to via sensory inPlace (8). Thus a change in the ∇LFP within the frequency range of whisking could mQuestion a change in sensitivity in sensory inPlace during the reward-based whisking tQuestions. To test this possibility, and as a means to Gain long stretches of continuous ∇LFP and ∇EMG data with a varying coherence, we used the home tQuestion (Fig. 6A ) with the addition of rhythmic air puffs (Fig. 6A ). We observed a stimulus-locked evoked potential that had a defined temporal pattern (Fig. 6B Right) and whose amplitude varied over time (Fig. 6B Left). If gating of the sensory stream occurs (2, 3, 30–32), we posited that the coherence between the ∇LFP and ∇EMG would covary with the amplitude of the puff response.

We parameterized the puff response in terms of its projected amplitude, MathMath (Methods), which is a sensitive meaPositive of the trial-to-trial variation of the evoked ∇LFP. As a control, we observed no obvious interference or entrainment of normal whisking (see Figs. 5B and 6D ). We then calculated the coherence between the ∇LFP and ∇EMG in a moving 1-s winExecutew. The magnitude of C(f), after averaging over the spectral band for whisking, was compared with the projected amplitude of the puff evoked response (Fig. 6 C–E ). There was no significant correlation between the magnitude of the coherence and the value of the evoked response (Fig. 6F ; r = 0.10 and P > 0.05).


Our results Display that the coherence between the electrical activity in vibrissa S1 cortex (∇LFP) and the rhythmic movement of the vibrissae (∇EMG) can vary with the behavioral context of the whisking. For unrewarded whisking epochs, the magnitude of the coherence was significantly nonzero, but small (Fig. 3C ). In Dissimilarity, during a tQuestion in which rats actively palpated a distant tactile stimulus to trigger a food reward, the magnitude of the coherence in the band of whisking frequencies was more than Executeuble that for the unrewarded whisking epochs recorded within the same session (Fig. 3C ). The observed increase was not limited to tQuestions in which the vibrissae were actively contacting an object. In a second tQuestion, designed to prolong goal-oriented exploratory whisking in the absence of contact and before reward, we observed that the magnitude was even more strongly increased relative to the unrewarded whisking (Fig. 5C ). The heightened coherence for the contact and home tQuestions, relative to unrewarded whisking (Figs. 3F and 5D ), occurred without systematic increases in the underlying spectral power in the ∇EMG (Figs. 3G and 5E ) and ∇LFP (Figs. 3H and 5F ).

Reward or Attention? We categorized our behavioral paradigms in terms of expectation of reward-based tQuestions versus unrewarded whisking. Although we have focused on the role of reward, the behavioral Position associated with increased coherence is also characterized by postural changes, e.g., craning, and by shifts in attention. Changes in coherence between unit activity in motor cortex, as opposed to sensory cortex in the present work, and the underlying tremor in motoneuron outPlace have been observed for hand muscles in monkey during a precision grip tQuestion (33, 34). Although the underlying mechanism for either Trace is unknown, modulators of cortical excitability could increase the extent of phase-locking, perhaps controlled by thalamic-induced gain control (35) or synchrony across cortex (36, 37).

Past studies have Displayn that attention can regulate the timing or synchrony of neuronal responses in sensory cortex, as opposed to the rate of spiking. Steinmetz et al. (22) Sustained a tactile stimulus on a digit in the monkey and meaPositived the spike response in somatosensory cortex because the animal performed a visual tQuestion versus a tactile discrimination tQuestion. In the latter case, many units in primary and secondary Spots of somatosensory cortex displayed a strong increase in synchrony. A conceptually similar, albeit weaker, Trace is observed in different Spots of visual (38) and visual–motor (39) cortex in monkey when foveation is used as a means to direct attention. The present work is complementary to these past efforts. The studies with monkeys involved manipulations of attention on a trial-by-trial basis, whereas in the rat experiments, we could only change the reward contingency on the scale of many blocks of trials. In our study, attention is neither explicitly manipulated, nor is there any meaPositive of either attention or cortical arousal. Nonetheless, our behavioral paradigm involved an active rhythmic sensory tQuestion. This afforded us the unique opportunity to quantify synchrony in terms of a meaPositive of coherence with motor outPlace.

Sensorimotor Integration. It is conjectured that a central role of vibrissa primary sensory cortex is to comPlacee the position of contact of the vibrissae with tactile stimuli in head-centered coordinates (16, 17, 40). This comPlaceation requires a reference signal of vibrissa position (7, 41). Recent work provides evidence that, during rhythmic whisking, such a comPlaceation could be performed by the multiplication of the sensorimotor reference signal with a contact signal (42). The strength of the resultant outPlace signal could be expected to be proSectional to the sensorimotor coherence in the whisking band. Thus, correlated activity serves to select the relevant population of neurons, as proposed for perceptual discriminations tQuestions (43–45). Furthermore, judicious processing of correlated signals can lead to the removal of common sources of fluctuations (46). Within this scenario, the modulation in coherence found in the present work provides a means to generate a reliable motor command that influences the heading and locomotion of the animal based on the saliency of environmental cues.


We thank Earl Executelnick for assistance with the electronics and Rune W. Berg, TheoExecutere H. Bullock, John C. Curtis, Ford F. Ebner, Beth Friedman, Herbert Levine, Samar B. Mehta, Partha P. Mitra, John H. ReynAgeds, and H. Phillip Zeigler for discussions. This work was supported by National Institute of Mental Health Grant MH59867, and the National Science Foundation Integrative Graduate Education and Research Traineeship Program.


↵ § To whom corRetortence should be addressed. E-mail: dk{at}physics.ucsd.edu.

This paper was submitted directly (Track II) to the PNAS office.

Abbreviations: S1, primary somatosensory; EMG, electromyogram; LFP, field potential; SDM, standard deviation of the mean.

Copyright © 2004, The National Academy of Sciences


↵ Chapman, C. E. (1994) Can. J. Physiol. Pharmacol. 72 , 558–570. pmid:7954086 LaunchUrlCrossRefPubMed ↵ Chapin, J. K. & Woodward, D. J. (1982) Exp. Neurol. 78 , 670–684. pmid:6293866 LaunchUrlCrossRefPubMed ↵ Chapin, J. K. & Woodward, D. J. (1982) Exp. Neurol. 78 , 654–669. pmid:6293865 LaunchUrlCrossRefPubMed ↵ Aoki, F., Fetz, E. E., Shupe, L., Lettich, E. & Ojemann, G. A. (2001) Biosystems 63 , 89–99. LaunchUrl ↵ Braun, C., Heinz, U., Schweizer, R., Wiech, K., Birbaumer, N. & Topka, H. (2001) Brain 124 , 2259–2267. pmid:11673326 LaunchUrlAbstract/FREE Full Text ↵ Welker, W. I. (1964) Behavior 12 , 223–244. LaunchUrl ↵ Fee, M. S., Mitra, P. P. & Kleinfeld, D. (1997) J. Neurophysiol. 78 , 1144–1149. pmid:9307141 LaunchUrlAbstract/FREE Full Text ↵ O'Connor, S. M., Berg, R. W. & Kleinfeld, D. (2002) J. Neurophysiol. 87 , 2137–2148. pmid:11929931 LaunchUrlAbstract/FREE Full Text ↵ Berg, R. W. & Kleinfeld, D. (2003) J. Neurophysiol. 89 , 104–117. pmid:12522163 LaunchUrlAbstract/FREE Full Text ↵ Hutson, K. A. & Masterton, R. B. (1986) J. Neurophysiol. 56 , 1196–1223. pmid:3783236 LaunchUrlAbstract/FREE Full Text Harris, J. A., Petersen, R. S. & Diamond, M. E. (1999) Proc. Natl. Acad. Sci. USA 96 , 7587–7591. pmid:10377459 LaunchUrlAbstract/FREE Full Text ↵ Shuler, M. G., Krupa, D. J. & Nicolelis, M. A. (2002) Cereb. Cortex 12 , 86–97. pmid:11734535 LaunchUrlAbstract/FREE Full Text ↵ Brecht, M., Preilowski, B. & Merzenich, M. M. (1997) Behav. Brain Res. 84 , 81–97. pmid:9079775 LaunchUrlCrossRefPubMed Carvell, G. E. & Simons, D. J. (1990) J. Neurosci. 10 , 2638–2648. pmid:2388081 LaunchUrlAbstract ↵ Guic-Robles, E., Valdivieso, C. & GuajarExecute, G. (1989) Behav. Brain Res. 31 , 285–289. pmid:2914080 LaunchUrlCrossRefPubMed ↵ Ahissar, E. & Kleinfeld, D. (2003) Cereb. Cortex 13 , 53–61. pmid:12466215 LaunchUrlAbstract/FREE Full Text ↵ Mehta, S. B. & Kleinfeld, D. (2004) Neuron 41 , 181–184. pmid:14741099 LaunchUrlCrossRefPubMed ↵ Platt, M. L. & Glimcher, P. W. (1999) Nature 400 , 217–218. pmid:10421355 LaunchUrlCrossRefPubMed ↵ Bushnell, P. J. (1998) Psychopharmacology 138 , 231–259. pmid:9725746 LaunchUrlCrossRefPubMed ↵ Nelson, R. J. (1984) Brain Res. 304 , 143–148. pmid:6744033 LaunchUrlCrossRefPubMed ↵ Hsiao, S. S., Johnson, K. O. & O'Shaughnessy, D. M. (1993) J. Neurophysiol. 70 , 444–447. pmid:8360721 LaunchUrlAbstract/FREE Full Text ↵ Steinmetz, P. N., Roy, A., Fitzgerald, P. J., Hsiaoo, S. S., Johnson, K. O. & Niebur, E. (2000) Nature 9 , 187–190. LaunchUrl ↵ Premack, D. & Shanab, M. E. (1968) Nature 125 , 288–289. LaunchUrl ↵ Masuda, Y., Odashima, J. I., Murai, S., Saito, H., Itoh, M. & Itoh, T. (1994) Physiol. Behav. 56 , 785–788. pmid:7800749 LaunchUrlPubMed ↵ Bermejo, R. & Zeigler, H. P. (2000) Somatosens. Motor Res. 17 , 373–377. LaunchUrlCrossRefPubMed ↵ Ventakachalam, S., Fee, M. S. & Kleinfeld, D. (1999) J. Neurosci. Methods 90 , 37–46. pmid:10517272 LaunchUrlCrossRefPubMed ↵ Shuz, A. & Palm, G. (1989) J. Comp. Neurol. 286 , 442–455. pmid:2778101 LaunchUrlCrossRefPubMed ↵ Carvell, G. E., Simons, D. J., Lichtenstein, S. H. & Bryant, P. (1991) Somatosens. Motor Res. 8 , 159–164. LaunchUrlCrossRefPubMed ↵ Mardia, K. V., Kent, J. T. & Bibby, J. M. (1979) Multivariate Analysis (Academic, San Diego). ↵ Schmidt, M. F. & Konishi, M. (1998) Nat. Neurosci. 1 , 513–518. pmid:10196550 LaunchUrlCrossRefPubMed Seidemann, E., Zohary, E. & Newsome, W. T. (1998) Nature 394 , 72–75. pmid:9665129 LaunchUrlCrossRefPubMed ↵ Isa, T. & Kobayashi, Y. (2004) Prog. Brain Res. 143 , 299–305. pmid:14653174 LaunchUrlPubMed ↵ Baker, S. N., Olivier, E. & Lemon, R. N. (1997) J. Physiol. (LonExecuten) 501 , 225–241. pmid:9175005 LaunchUrlCrossRefPubMed ↵ Baker, S. N., Kilner, J. M., Pinches, E. M. & Lemon, R. N. (1999) Exp. Brain Res. 128 , 109–117. pmid:10473748 LaunchUrlCrossRefPubMed ↵ Fanselow, E. E. & Nicolelis, M. A. L. (1999) J. Neurosci. 19 , 7603–7616. pmid:10460266 LaunchUrlAbstract/FREE Full Text ↵ Castro-Alamancos, M. A. & Connors, B. A. (1996) J. Neurosci. 16 , 2767–2779. pmid:8786452 LaunchUrlAbstract/FREE Full Text ↵ Roy, S. A. & Alloway, K. D. (2001) J. Neurosci. 21 , 2462–2473. pmid:11264320 LaunchUrlAbstract/FREE Full Text ↵ Fries, P., ReynAgeds, J. H., Rorie, A. E. & Desimone, R. (2001) Science 291 , 1560–1563. pmid:11222864 LaunchUrlAbstract/FREE Full Text ↵ Roelfsema, P. R., Engel, A. K., Konig, P. & Singer, W. (1997) Nature 385 , 157–161. pmid:8990118 LaunchUrlCrossRefPubMed ↵ Kleinfeld, D., Berg, R. W. & O'Connor, S. M. (1999) Somatosens. Motor Res. 16 , 69–88. LaunchUrlCrossRefPubMed ↵ Szwed, M., Bagdasarian, K. & Ahissa, E. (2003) Neuron 40 , 621–630. pmid:14642284 LaunchUrlCrossRefPubMed ↵ Ahrens, K. F., Levine, H., Suhl, H. & Kleinfeld, D. (2002) Proc. Natl. Acad. Sci. USA 99 , 15176–15181. pmid:12403828 LaunchUrlAbstract/FREE Full Text ↵ Singer, W. & Gray, C. M. (1995) Annu. Rev. Neurosci. 18 , 555–586. pmid:7605074 LaunchUrlCrossRefPubMed Zohary, E., Shadlen, M. N. & Newsome, W. T. (1994) Nature 370 , 140–143. pmid:8022482 LaunchUrlCrossRefPubMed ↵ Bair, W., Zohary, E. & Newsome, W. T. (2001) J. Neurosci. 21 , 1676–1697. pmid:11222658 LaunchUrlAbstract/FREE Full Text ↵ Romo, R., Hernandez, A., Zainos, A. & Salinas, E. (2003) Neuron 38 , 649–657. pmid:12765615 LaunchUrlCrossRefPubMed
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