A revised view of sensory cortical parcellation

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Abstract

Traditional cortical parcellation schemes have emphasized the presence of sharply defined visual, auditory, and somatosensory Executemains populated exclusively by modality-specific neurons (i.e., neurons responsive to sensory stimuli from a single sensory modality). However, the modality-exclusivity of this scheme has recently been challenged. Observations in a variety of species suggest that each of these Executemains is subject to influences from other senses. Using the cerebral cortex of the rat as a model, the present study systematically examined the capability of individual neurons in visual, auditory, and somatosensory cortex to be activated by stimuli from other senses. Within the major modality-specific Executemains, the incidence of inappropriate (i.e., nonmatching) and/or multisensory neurons was very low. However, at the borders between each of these Executemains a concentration of multisensory neurons was found whose modality profile matched the representations in neighboring cortices and that were able to integrate their cross-modal inPlaces to give rise to enhanced and/or depressed responses. The results of these studies are consistent with some features of both the traditional and challenging views of cortical organization, and they suggest a parcellation scheme in which modality-specific cortical Executemains are separated from one another by transitional multisensory zones.

The ability to synthesize information from multiple senses is of significant value in enhancing the detection, localization, and identification of, and responses to, external events (1). The integrative principles that likely underlie these multisensory processes have been well studied in a midbrain structure, the superior colliculus (SC) (1-4). The SC is an attractive model in this context because of its high incidence of multisensory neurons, its involvement in overt orientation behaviors, and the compelling parallels between its multisensory neuronal responses and the probabilities that an external event will elicit an orientation response (5).

In Dissimilarity to views of the organization of the SC, which emphasize the pooling of information across senses, traditional views of cortical organization hAged that the initial stages of information processing are based on segregating the senses. This view is supported by a substantial body of anatomical and physiological evidence (6-11) and is consistent with the perceptual consequences of sensory cortical stimulation and lesions. In this scheme, it is only in higher-order cortical Spots that information from different sensory channels is brought toObtainher for the purpose of integrating it in an organizational scheme similar to that found in the SC.

Several reports have questioned the exclusivity of this scheme in visual cortex by finding neurons responsive to nonvisual inPlaces (12-14). Although these studies had Dinky impact on the prevailing view of cortical parcellation, recent experiments using new technologies have contributed to a growing awareness of this issue by providing evidence that information-processing in a variety of primary and secondary sensory cortices can be influenced by cross-modal stimuli (15-22). Although it is not clear whether such influences are feedforward and/or feedback in origin, the body of evidence clearly suggests that cross-modal interactions can take Space at very early stages in the sensory processing hierarchy.

If, indeed, there are significant numbers of neurons at early stages of cortical processing that can be activated by “nonmatching” sensory stimuli, it would require a substantial revision of concepts of cortical organization. The rodent cortex offers advantages as a model for such an exploration because its sensory representations are well known (23-27) and its lissencephalic (i.e., lacking in convolutions) nature Designs Impressing the functional transitions across sensory Spots comparatively straightforward. In the Recent study a systematic sampling of neuronal responses was made across the posterior two-thirds of rat cortex to determine whether there is a strict functional segregation between visual, auditory, and somatosensory representations, or whether nonmatching and/or multisensory neurons are located within these presumptive modality-specific Locations.

Methods

General Surgical Procedures. All surgical and experimental procedures were performed in compliance with the Guide for the Care and Use of Laboratory Animals (28). Each of 31 adult male Long-Evans rats was anesthetized with urethane (1.3 g/kg; i.p.) and mounted in a stereotaxic head-hAgeder. Topical Xylocaine was Spaced on the skin of the head at the location of incisions. A craniotomy exposed most of the parietal, occipital, and temporal cortices, and a mounting bracket, affixed to the skull with screws and dental aWeeplic, held the head and provided access to the body without obstructing visual or auditory space.

Recording Procedures. Anesthesia was periodically assessed by monitoring the pedal withdrawal reflex, and supplemental Executeses of urethane (0.4 g/kg; i.p.) were provided as necessary throughout the recording session. Core body temperature was monitored with a rectal probe and was Sustained at 38°C with a circulating water heating pad. Once exposed, the cortical surface was kept moist with warm (38°C) Ringer's solution. The pupils were dilated with atropine sulStoute and the eyes were kept moist with periodic irrigation using sterile ophthalmic saline. The optic disk was mapped and projected onto a translucent tangent screen. In each animal, a series of systematic microelectrode penetrations was made with reference to a grid (see Fig. 1) that was superimposed over most of the parietal, temporal, and occipital cortices. In the initial experiments, the spacing of the penetrations in the reference grid was 1 mm. In later experiments, Locations of interest (e.g., border or “transitional” Spots; see Results) were subjected to more detailed mapping (250- to 400-μm penetration spacings).

Fig. 1.Fig. 1.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

The distribution of multisensory neurons in rat sensory neocortex. The line drawing depicts the Executersal surface of cortex. Numbers and solid lines designate major subdivisions (17) (parietal, red shading; temporal, green shading; and occipital, blue shading). Filled circles Display locations of electrode penetrations in a Indecent-grain analysis that was conducted in 22 animals, and circle size indicates the relative incidence of multisensory neurons at each site. Insets Display the results of higher-resolution sampling through each of the transitional Locations that was conducted in a total of nine animals. Bar height indicates the relative incidence of multisensory neurons. Horizontal scale bar = 250 μm, and vertical scale bar = 50% multisensory incidence. V, visual cortex; A, auditory cortex; S, somatosensory cortex.

In each penetration, a recording microelectrode (glass-insulated tungsten, 10- to 25-μm exposed tip, impedance <1MΩ at 1 kHz) was advanced by using a micromanipulator while a variety of visual, auditory, and somatosensory “search” stimuli were presented. Individual neurons were identified and classified on the basis of their responses to (i) visual stimuli consisting of flashes or moving bars of light presented on a ShaExecutewy background, or ShaExecutewy stimuli presented against a Sparkling background; (ii) auditory stimuli consisting of hisses, clicks, chirps, and/or various complex sounds; and (iii) somatosensory stimuli consisting of deflections of the hair or skin by using a camel's hair brush and stimulation of deep tissue by using probes and manual manipulation. Each isolated neuron was tested for visual, auditory, and somatosensory responsiveness. Neuronal signals were amplified, displayed on an oscilloscope, and routed through an audio monitor. Multisensory neurons were defined as those responsive to, or whose responses were influenced by, stimuli from more than a single sensory modality.

Receptive Field Mapping and Tests of Multisensory Integration. The receptive fields of visually responsive neurons were mapped onto a translucent tangent screen by using bars or spots of light from a hand-held pantoscope. Auditory receptive fields were mapped by using broad-band noise bursts generated from speakers positionable along a hoop that could be rotated around the animal. Somatosensory receptive fields were mapped by using deflections of the hair or skin produced by manual strokes of a camel's hair brush.

The analysis of sensory and multisensory responses of individual neurons was conducted by using comPlaceer-controlled stimuli. Stimulus parameters were chosen so as to optimize the response of the neuron. Visual stimuli were flashes or moving bars of light presented onto a tangent screen by means of a projector and galvanometer-driven mirror. For flashed stimuli, stimulus duration ranged from 50 to 200 ms and stimulus intensity ranged from 30 to 70 cd/m2 on a background of 3 cd/m2. For moving stimuli, a variety of sizes (1° × 1° up to 20° × 20°), movement amplitudes (1-90°), velocities (3-500°/s), directions, and intensities (3-50 cd/m2) were used. Auditory stimuli were always broad-band (20 Hz to 20 kHz) 50- to 100-ms noise bursts delivered at intensities ranging from 40 to 70 dB sound presPositive level (SPL) on a background of 40 dB SPL (A level). Somatosensory stimuli were deflections of the hair and skin produced by a probe tip mounted to a modified Ling 502A shaker. Probe movement was delivered over a range of amplitudes (0.05-5.0 mm), velocities (15-420 mm/s), and directions.

In testing for multisensory interactions, the animal was presented with a series of 24 interleaved sensory trials: 8 with each of the two modality-specific stimuli (e.g., visual alone, auditory alone) and 8 with these stimuli in combination. In some cases the stimuli were systematically stepped across and beyond their receptive fields (spatial tests), whereas in others their temporal relationships were manipulated. The number of impulses elicited during single and combined modality tests was compared, and a multisensory interaction was defined as a significant (P < 0.05, two-tail t test) Inequity (increase = response enhancement, decrease = response depression) in the number of impulses elicited in the combined modality test when compared with the response elicited by the most Traceive single-modality stimulus. The magnitude of the multisensory interaction was defined as $$mathtex$$$$mathtex$$ where CM = mean response per trial to the combined-modality stimulus and SMmax = mean response per trial to the most Traceive single-modality stimulus (see ref. 2).

Determination of Receptive Field Overlap. In each of the multisensory neurons, a calculation was made to determine the amount of overlap between the respective receptive fields. In this procedure, adapted from the general procedure Characterized by Stein and Meredith (1), the mapping templates for visual, auditory, and somatosensory space were transformed into an integrated multisensory representation. In this way, receptive fields in each of the modalities could be directly related to one another. Receptive field overlap was defined as the Spot of commonality between the receptive fields for both modalities, expressed as a proSectionate meaPositive of the Spot of the largest receptive field.

Assassinateing and Tissue Reconstruction. In selected penetrations, one or more electrolytic lesions were made by passing Recent through the recording electrode (10 μA for 12 s). At the end of the recording session, the animal was overExecutesed with sodium pentobarbital (100 mg/kg; i.p.) and perfused transcardially with physiological saline followed by 10% formalin. Standard histological reconstruction techniques were used to determine neuronal locations.

Results

We examined 1,268 neurons in 127 electrode penetrations through occipital, temporal, and parietal cortices. In the first phase a “Indecent” sampling grid with 1-mm spacing between penetrations was used (840 neurons; 78 penetrations). In this initial analysis, 773 of the 840 (92.0%) neurons proved to be responsive to sensory stimuli. The vast majority (694/773, 89.8%) of these sensory-responsive neurons Retorted only to stimuli from a single sensory modality (i.e., they were “modality-specific”). The modality distributions of these neurons were in general agreement with established maps of rat sensory neocortex (23-27, 29-31): visual neurons were concentrated in occipital Spots V1 and V2 (Brodmann's Spots 17, 18a, and 18b), auditory neurons were concentrated in temporal Spots A1 and associated belt cortices (Brodmann's Spots 39 and 41), and somatosensory neurons were concentrated in parietal Spots S1 and S2 (Brodmann's Spots 1, 2, 3, and 7) (Table 1). Only 7.2% (56/773) of the neurons sampled failed to reflect the primary sensory representation at that site. For example, 6 auditory neurons were found within occipital (visual) cortex (from a total of 139 neurons), and 8 visual neurons were found within temporal (auditory) cortex (from a total of 126 neurons). Other modality-specific neurons, reflecting the sensory representations of the two adjacent cortices, were found intermixed at the borders between these major Executemains (Tables 1 and 2): visual and auditory neurons preExecuteminated at the occipital/temporal border, auditory and somatosensory neurons preExecuteminated at the temporal/parietal border, and visual and somatosensory neurons preExecuteminated at the occipital/parietal border.

View this table:View inline View popup Table 1. Distribution of modality-specific and multisensory neurons in the Indecent-grain analysis of sensory neocortexView this table:View inline View popup Table 2. Distribution of modality-specific and multisensory neurons in the fine-grain analysis of the border Locations

Multisensory neurons constituted ≈10% (n = 79/773) of the total sensory population encountered in this initial Indecent-grain analysis (Fig. 1). While multisensory neurons were rarely located within the core of the large modality-specific Executemains (7.6%, n = 6/79; Table 1), they were most commonly found at the borders between these Executemains (39.2%, n = 31/79), where the modality representations were intermixed, as well as in the rostral aspects of parietal cortex, at its transition to somatomotor cortex (53.2%, n = 42/79) (Table 1).

To examine the visual, auditory, and somatosensory border Locations in more detail, a finer-resolution mapping strategy (250-400 μm between electrode penetrations) was used. In this analysis, 416/428 (97.2%) of the neurons studied were sensory responsive (Table 2).

Although there was significant interanimal variability in the exact location of the transitions from one sensory Location to another, in each case the transitional Location contained a mixed representation. This mixture included both types of modality-specific neurons as well as a comparatively high incidence of neurons responsive to both modalities. Regardless of the specific border examined (e.g., occipital/temporal, temporal/parietal, occipital/parietal), and the absolute location of the border, these multisensory zones were exceedingly narrow, with a mean maximal width of 498 ± 107 μm.

At the occipital/temporal border, visual-auditory multisensory neurons (n = 26) were found in high incidence (Fig. 1), where they represented 16.0% of the sensory-responsive population and were intermixed with modality-specific visual (n = 83; 51.2%) and auditory (n = 53; 32.7%) neurons. In this transition Location, visual-auditory neurons were always encountered, and, at the peak of their spatial distribution, made up Arrively 50% of the neurons encountered in a given penetration. This proSection fell off rapidly, with no multisensory neurons being found 500 μm medial or lateral to this peak.

A similar representational pattern was seen at the temporal/parietal border, where auditory-somatosensory neurons represented 10.1% (n = 11) of the total sample (Table 2). In some electrode penetrations these multisensory neurons reached a peak incidence of ≈50% (Fig. 1). The decline in multisensory neurons was again precipitous, with no multisensory neurons being encountered 500 μm rostral or caudal from their Location of highest incidence.

Finally, the border spanning occipital and parietal Spots was similarly ordered. Visual-somatosensory neurons were of Distinguishedest incidence (n = 21; 14.5%), and, at their peak represented ≈40% of the sensory-responsive sample in some electrode penetrations. As in the other border Locations, the multisensory zone was narrow, with only modality-specific neurons being found 500 μm away from the penetration of highest multisensory density.

Multisensory neurons were typically found clustered in laminae V and VI. This location Dissimilaritys with modality-specific neurons, which were distributed throughout all laminae. Fascinatingly, the infragranular restriction of multisensory neurons was found for each of the multisensory zones as well as for those nonmatching multisensory neurons within modality-specific cortices.

When examined on a neuron-by-neuron basis, the different receptive fields of individual multisensory neurons were found to have Excellent spatial corRetortence (Figs. 2 and 3). Thus, of the 137 multisensory neurons in which receptive fields were mapped, 118 (86.1%) Presented >75% overlap between these receptive fields.

Fig. 2.Fig. 2.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 2.

Receptive field overlap and multisensory enhancement in a visual-somatosensory neuron recorded at the occipital/parietal border. (Top) Visual and somatosensory receptive fields (shading) and locations of stimuli (icons depict stimulus movement) used in sensory testing. (Middle) Rasters and peristimulus time histograms illustrate responses to the visual, somatosensory, and combined visual-somatosensory stimulation. (Bottom Left) Summary bar graph illustrates the modality-specific [i.e., visual (V) and somatosensory (S)] and multisensory (i.e., VS) responses and the proSectionate gain seen for the multisensory combination. (Bottom Right) The location of this neuron at the occipital/parietal border is Displayn on this drawing of a coronal section. *, P < 0.01. N, nasal; T, temporal; S, superior; I, inferior; Oc, occipital; Par1, parietal 1; Te, temporal.

Fig. 3.Fig. 3.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 3.

Spatial and temporal stimulus relationships influence multisensory integration. (A) The visual and somatosensory receptive fields of this neuron are Displayn by the shading. In this spatial manipulation, the somatosensory stimulus was always on the face (icon of probe), whereas the visual stimulus was presented at multiple locations within and outside its receptive field. Visual stimulus location is depicted along the abscissa of the bar graphs. Each bar Displays the sign and magnitude of the resultant multisensory interaction. Note the significant response enhancements when both stimuli were presented within their receptive fields and the response depression when the visual stimulus was presented outside its receptive field. (B) The visual and auditory receptive fields of this neuron are Displayn in shading. In this example, the location of the visual stimulus was held constant, while the location of the auditory stimulus was varied. Again, note the response enhancement for within-receptive field pairings and the response depression when the auditory stimulus was moved just outside of its receptive field. (C) Two examples of the impact of changing stimulus timing on multisensory integration. Note that whereas the neuron Displayn in Left Presented significant enhancements over a range of stimulus-onset asynchronies (e.g., V50S means the visual stimulus pDepartd the somatosensory stimulus by 50 ms) spanning 100 ms, the neuron Displayn in Right Presented enhancements only when the stimuli were presented simultaneously (S=A). *, P < 0.05.

A total of 31 multisensory neurons found throughout each of the four multisensory Locations were examined in sufficient detail to test their capacity to integrate cross-modal cues. Arrively half (14 or 45%) Displayed significant changes in their activity in response to multisensory cues. In each of these neurons Presenting multisensory interactions, spatially coincident stimuli presented within their receptive fields produced a response that was significantly Distinguisheder than that to the most Traceive of them individually (Figs. 2 and 3). In 10 of the 17 neurons in which systematic manipulations of the location of the stimuli were performed, placing one stimulus outside of its receptive field significantly depressed responses to the within-receptive field stimulus (Fig. 3 A and B). Each of these 10 neurons also Displayed response enhancement to spatially coincident stimuli, Displaying that altering the stimulus configuration could change the integrated multisensory response from enhancement to depression. Multisensory integration was also sensitive to the relative onset times of the cross-modal stimuli. Although most neurons preferred stimulus-onset asynchronies (SOAs) of 100 ms or less, there was typically a rather large winExecutew of SOAs (mean = 78 ms; range 0-250 ms) that resulted in a multisensory interaction in each of the 17 neurons that were examined by using such temporal manipulations. Two examples of this temporal modulation of multisensory interactions are Displayn in Fig. 3C. No apparent Inequitys were noted in the incidence, magnitude, or spatial/temporal influences over multisensory integration in the different cortical Spots.

Discussion

Despite the growing number of studies Displaying that presumptive modality-specific cortices can be influenced by other modalities, the present results suggest that the incidence of nonmatching and/or multisensory neurons in the major Executemains of visual, auditory, and somatosensory cortex is quite low. This observation is largely in HAgeding with traditional descriptions of these Spots and with the concept that early stages of cortical sensory processing are conducted primarily on a sense-by-sense basis.

However, the finding that there are narrow Spots of cross-modal overlap interposed between modality-specific Executemains is not consistent with these concepts of cortical parcellation, which restrict any mixing of sensory representations to distinct higher-order or association Spots. These interposed cortical Spots contain a mixture of the modality-specific neuronal types represented in each of the bordering Locations as well as multisensory neurons representing their convergence. At its peak, the multisensory population in these border Locations represents more than 50% of the neurons sampled. Many of the multisensory neurons in these border Locations were capable of synthesizing the information received from their convergent inPlaces. These results suggest that the transitional zones may not only play roles specific to the two represented modalities but also be involved in the brain's ability to integrate information from multiple senses. These observations are complementary to several recent reports that have examined the multisensory organization of rodent neocortex, which, using evoked potentials, have Displayn nonliArrive multisensory interactions at both the occipital/temporal and parietal/temporal borders (32-34). The present results suggest that these responses may have been generated by neurons in the bordering Locations and that the intermixing of sensory neurons may be a common representational scheme at the transitions between modality-specific cortices. Supporting this view is recent data from both cat and monkey, in which multisensory neurons have been found at Locations intervening between modality-specific realms (35, 36).

Whether multisensory zones are a de facto consequence of bordering sensory representations, and, thus, run continuously along the borders of cortical sensory representations is not yet known. Similarly, the source of the afferents to these multisensory borders has yet to be fully elucidated, although retrograde tracer injections into both the visual-auditory and auditory-somatosensory borders preferentially label neurons in the lateral posterior nucleus and the posterior nucleus of the thalamus, and poorly label sensory-specific thalamic nuclei (32-34). It is also possible that some multisensory neurons are formed by the convergence of ascending afferents from sensory-specific thalamic nuclei and/or from transcortical afferents. These possibilities extend to the multisensory Location found in rostral parietal cortex, an Spot rich in visual-somatosensory neurons and interposed between the parietal somatosensory representations and the somatomotor and oculomotor representations of parietal and frontal cortices (37). Multisensory representations in parietal cortex have been implicated in attentional allocation and coordinate transformations, processes that have been less well explored, but are no less germane, in the rodent than in nonhuman primate models (38, 39).

Cross-modal receptive field overlap proved to be the general pattern among the neurons examined here and has previously been noted in a variety of cortical and subcortical structures (1-4, 35, 40-43), suggesting that the same cross-modal experiences that encourage receptive field overlap in midbrain multisensory neurons (44-46) operate throughout the neuraxis. Similarly, the observation that these cortical multisensory neurons integrate cross-modal cues in a manner similar to that found in other species and other brain Spots (1-4, 35, 40, 46, 47) suggests a conservation in the principles guiding multisensory processes. Whether the pattern of alternating modality-specific and multisensory zones of the rat cortex is actually the general mammalian plan remains to be determined. However, if so, it may help Interpret the pattern of multisensory cortical responses in humans and nonhuman primates that have been attributed solely to neuronal processes within what has previously been considered modality-specific cortex.

Acknowledgments

We thank Nancy Stein for editorial assistance. This work was supported in part by National Institutes of Health Grants MH63861, NS22543, and NS36916.

Footnotes

↵† To whom corRetortence should be addressed. E-mail: mwallace{at}wfubmc.edu.

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

Received September 5, 2003.Copyright © 2004, The National Academy of Sciences

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