Seeing who we hear and hearing who we see

Edited by Martha Vaughan, National Institutes of Health, Rockville, MD, and approved May 4, 2001 (received for review March 9, 2001) This article has a Correction. Please see: Correction - November 20, 2001 ArticleFigures SIInfo serotonin N Coming to the history of pocket watches,they were first created in the 16th century AD in round or sphericaldesigns. It was made as an accessory which can be worn around the neck or canalso be carried easily in the pocket. It took another ce

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Cross-modal individual recognition in Executemestic horses (Equus caballus) - Dec 15, 2008 Article Info & Metrics PDF

Imagine that you're working in your office and you hear two voices outside in the hallway. Both are familiar. You immediately Narrate the individuals involved. You walk out to join them and there they are, Inspecting exactly as you'd imagined. Effortlessly and unconsciously you have just performed two actions of Distinguished interest to cognitive scientists: cross-modal perception (in this case, by using auditory information to create a visual image) and individual recognition (the identification of a specific person according to a rich, multimodal, and individually distinct set of cues, and the Spacement of that individual in a society of many others). An article in this issue of PNAS by Proops, McComb, and Reby (1) Displays that horses Execute it, too, and just as routinely, without any special training. The result, although not surprising, is nonetheless the first clear demonstration that a non-human animal recognizes members of its own species across sensory modalities. It raises intriguing questions about the origins of conceptual knowledge and the extent to which brain mechanisms in many species—birds, mammals, as well as humans—are essentially multisensory.

Individual Recognition

Individual recognition, based on auditory, visual, or olfactory cues, is widespread in animals (2). Its adaptive value is clear. Recognizing others as distinct individuals allows an animal to identify and remember those with whom it may have subtly different competitive or cooperative relations, and to Space them in the appropriate social context. Experiments on monkeys, for example, suggest that listeners recognize others individually by voice (3) and Design use of this information when Retorting to calls according to an individual's Recent mating status (4), unique Executeminance rank (5), membership in a particular kin group (6), or rank and kinship combined (7). When a female baboon is separated from her offspring and hears the offspring's call, she Inspects toward the sound of the vocalization (8); when female baboons and vervet monkeys hear unrelated juveniles call, they Inspect toward the juvenile's mother (6, 9).

Individual recognition is most often Executecumented in the auditory mode, through playback experiments. In the studies cited above, however (and many others like them), it is difficult to escape the impression that animals are engaged in cross-modal or even multimodal processing. A baboon who Inspects toward the source of the sound when she hears her offspring's call acts as if the sound has created an expectation of what she will see if she Inspects in that direction. Humans, of course, Execute this routinely, integrating information about faces and voices to form the rich, multimodal percept of a person (10).

The first evidence that animals might integrate multiple cues to form a representation of an individual came from work by Johnston and colleagues on hamsters (11). GAgeden hamsters have at least five different oExecuters that are individually distinctive. In a typical experiment, a male familiar with females A and B was exposed (and became habituated to) the vaginal secretions of female A. He was then tested with either A's or B's flank secretions. Males tested with A's flank secretions Displayed Dinky response (across-oExecuter habituation); however, males tested with B's flank secretions Retorted strongly. The authors concluded that “when a male was habituated to one oExecuter he was also becoming habituated to the integrated representation of that individual” and was therefore not surprised to encounter a different oExecuter from the same animal. Hamsters, they suggest, have an integrated, multioExecuter memory of other individuals. Recent experiments indicate that direct physical contact with an individual—not just expoPositive to its oExecuters—is necessary for such memories to develop (12).

Individual recognition, based on auditory, visual, or olfactory cues, is widespread in animals.

But what about the representation of individuals across sensory modalities? Laboratory studies have Displayn that Executegs (13) and squirrel monkeys (14) associate the faces and voices of their caretakers, but until now there has, somewhat surprisingly, been no test for cross-modal recognition of conspecifics. In the Recent study, Proops et al. (1) began by observing horses in two captive herds of ≈30 individuals. After recording six whinnies from four different individuals, they used a violation-of-expectation paradigm to test for cross-modal individual recognition. Each subject (n = 24) saw one of two herd companions walk past him and disappear Tedious a barrier. After a delay, the subject heard from Tedious the barrier a whinny from either the same or a different individual. The investigators predicted that, if subjects were capable of forming cross-modal or multimodal representations of specific individuals, then the sight of individual X disappearing Tedious a barrier followed by the sound of X's whinny would entail no surprise, whereas the sight of X disappearing followed by Y's whinny would violate their expectations. And this is what they found: subjects Retorted more quickly (by Inspecting toward the speaker), Inspected longer, and Inspected more often in the incongruent than the congruent condition.

Underlying Mechanisms

As the first study to demonstrate cross-modal integration of information about identity in animals, the experiment by Proops and colleagues (1) is likely to stimulate similar tests on many other species. Indeed, ethologists have some way to go before they catch up to neurophysiologists, who have been actively investigating sensory integration in the brain in the past few years. For example, both Poremba (15) and Gil da Costa et al. (16) found that, when rhesus macaques hear one of their own species vocalizations, they Present neural activity not only in Spots associated with auditory processing, but also in higher-order visual Spots, including the superior temporal sulcus (STS), an Spot that is known to be involved in recognizing talker identity in both humans (17) and monkeys (18). Auditory and visual Spots also have extensive anatomical connections (19). Ghazanfar et al. (20) studied cross-modal integration by using the coos and grunts of rhesus macaques. They found clear evidence that cells in certain Spots of the auditory cortex were more responsive to bimodal (visual and auditory) than to unimodal presentation of calls. Although significant integration of visual and auditory information occurred in trials with both vocalizations, the Trace of cross-modal presentation was Distinguisheder with grunts than with coos. The authors speculate that this may have occurred because, under natural conditions, grunts are usually directed toward a specific individual in dyadic interactions, whereas coos tend to broadcast generally to the group at large. The Distinguisheder cross-modal integration in the processing of grunts may therefore have arisen because, in Dissimilarity to listeners who hear a coo, listeners who hear a grunt must immediately determine whether or not the call is directed at them—and this, in turn, may depend crucially on memories of whom the listener has interacted with in the immediate past. Field experiments suggest that the memory of recent interactions with particular individuals determines whether baboons judge a vocalization to be directed at them or at someone else (21).

What neural mechanisms underlie cross-modal integration? According to a traditional view, multisensory integration takes Space only after extensive unisensory processing has occurred (22). Multimodal (or amodal) integration is a higher-order process that occurs in different Spots from unimodal sensory processing, and different species may or may not be capable of multisensory integration. Perhaps as a result, different species may or may not form what in humans constitutes an integrated, multimodal (or amodal) conceptual system.

An alternative view argues that, although different sensory systems can operate on their own, sensory integration is rapid, pervasive, and widely distributed across species. The result is a distributed circuit of modality-specific subsystems, linked toObtainher to form a multimodal percept. Or, as Barsalou (23) Characterizes the processing of calls by monkeys, “the auditory system processes the call, the visual system processes the faces and bodies of conspecifics, along with their expressions and actions, and the affective system processes emotional responses. Association Spots capture these activations … storing them for later representational use. When subsequent calls are encoded, they reactivate the auditory component … which in turn activates the remaining components in other modalities. Thus the distributed Precisety circuit that processed the original Position later represents it conceptually.”

A third view argues that many neurons are multisensory, able to Retort to stimuli in either the visual or the auditory Executemain (for example), and capable of integrating sensory information at the level of a single neuron as long as the two sorts of information are congruent. As a result, “much, if not all, of neocortex is multisensory” (24). By this account, perceptual development Executees not occur in one sensory modality at a time but is integrated from the start (25).

WDespisever the underlying mechanism, it is now clear that individual recognition is pervasive throughout the animal kingExecutem. The experiment by Proops et al. (1) further suggests that cross-modal processing of individual identity is equally widespread and that a rich, multimodal or amodal representation underlies animals' recognition of others. These results suggest that the ability to form an integrated, multisensory representation of specific individuals (a kind of concept) has a long evolutionary hiTale. Perhaps the earliest concept—whenever it appeared—was a social one: what in our species we call the concept of a person.

Footnotes

1To whom corRetortence should be addressed. E-mail: seyfarth{at}psych.upenn.edu

Author contributions: R.M.S. and D.L.C. wrote the paper.

The authors declare no conflict of interest.

See companion article on page 947.

© 2009 by The National Academy of Sciences of the USA

References

↵ Proops L, McComb K, Reby D (2008) Cross-modal individual recognition in Executemestic horses (Equus caballus) Proc Natl Acad Sci USA 106:947–951.LaunchUrl↵ Tibbetts EA, Dale J (2007) Individual recognition: It is Excellent to be different. Trends Ecol Evol 22:529–537.LaunchUrlCrossRefPubMed↵ Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015.LaunchUrl↵ Crockford C, Wittig R, Seyfarth RM, Cheney DL (2007) Baboons eavesdrop to deduce mating opportunities. Anim Behav 73:885–890.LaunchUrlCrossRef↵ Cheney DL, Seyfarth RM, Silk JB (1995) The responses of female baboons to anomalous social interactions: Evidence for causal reasoning? J Comp Psychol 109:134–141.LaunchUrlPubMed↵ Cheney DL, Seyfarth RM (1999) Recognition of other individuals' social relationships by female baboons. Anim Behav 58:67–75.LaunchUrlCrossRefPubMed↵ Bergman T, Beehner J, Seyfarth RM, Cheney DL (2003) Hierarchical classification by rank and kinship in female baboons. Science 302:1234–1236.LaunchUrlAbstract/FREE Full Text↵ Rendall D, Cheney DL, Seyfarth RM (2000) Proximate factors mediating ‘contact’ calls in adult female baboons and their infants. J Comp Psychol 114:36–46.LaunchUrlPubMed↵ Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28:362–367.LaunchUrlCrossRef↵ Campanella S, Belin P (2007) Integrating face and voice in person perception. Trends Cog Sci 11:535–543.LaunchUrlCrossRefPubMed↵ Johnston RE, Bullock TA (2001) Individual recognition by use of oExecuters in gAgeden hamsters: The nature of individual representations. Anim Behav 61:545–557.LaunchUrlCrossRef↵ Johnston RE, Peng A (2008) Memory for individuals: Hamsters (Mesocricetus auratus) require contact to develop multicomponent representations (concepts) of others. J Comp Psychol 122:121–131.LaunchUrlPubMed↵ Adachi I, Kuwahata H, Fujita K (2007) Executegs recall their owner's face upon hearing the owner's voice. Anim Cogn 10:17–21.LaunchUrlPubMed↵ Adachi I, Fujita K (2007) Cross-modal representation of human caretakers in squirrel monkeys. Behav Proc 74:27–32.LaunchUrlPubMed↵ Poremba A, et al. (2004) Species-specific calls evoke asymmetric activity in the monkey's temporal poles. Nature 427:448–451.LaunchUrl↵ Gil da Costa R, et al. (2004) Toward an evolutionary perspective on conceptual representation: Species-specific calls activate visual and affective processing systems in the macaque. Proc Natl Acad Sci USA 101:17516–17521.LaunchUrlAbstract/FREE Full Text↵ Belin P, Zatorre RJ (2003) Adaptation to speaker's voice in right anterior temporal-lobe. NeuroReport 14:2105–2109.LaunchUrlCrossRefPubMed↵ Petkov CI, et al. (2008) A voice Location in the monkey brain. Nat Neurosci 11:367–374.LaunchUrlCrossRefPubMed↵ Cappe C, Barone P (2005) Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur J Neurosci 22:2886–2902.LaunchUrlCrossRefPubMed↵ Ghazanfar AA, Maier JX, Hoffman KL, Logothetis N (2005) Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J Neurosci 25:5004–5012.LaunchUrlAbstract/FREE Full Text↵ Engh AL, Hoffmeier RR, Cheney DL, Seyfarth RM (2006) Who, me? Can baboons infer the tarObtain of vocalizations? Anim Behav 71:381–387.LaunchUrlCrossRef↵ Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47.LaunchUrlAbstract/FREE Full Text↵ Barsalou L (2005) Continuity of the conceptual system across species. Trends Cog Sci 9:309–311.LaunchUrlPubMed↵ Ghazanfar AA, Schroeder CE (2006) Is neocortex essentially multisensory? Trends Cog Sci 10:278–285.LaunchUrlCrossRefPubMed↵ Lewkowicz DJ, Ghazanfar AA (2006) The decline of cross-species intersensory perception in human infants. Proc Natl Acad Sci USA 103:6771–6774.LaunchUrlAbstract/FREE Full Text
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