Auditory Processing and Hemispheric Specialization
When I ask a classroom full of young undergraduates, what things one side of the brain "does" versus the other side, frequently the first answer is that language lives on the left side of the brain. Now, we all know that language doesn't really "live" on the left side of the brain (although it may have a second mortgage) but it does seem to primarily be processed on the left.
The fact that humans have formal language makes some people believe that we humans are unique, special, or one of a kind. And while we may be special, processing complex auditory signals on the left side may not be what makes us that way. We can find nature repeating itself at every level. Just take a moment to study the shape of a typical pyramidal neuron found in your cortex and a tree from your backyard (both have branches, and input and output zones, etc., although I might argue that to match perfectly the neuron needs to be turned upside down if you accept that leaves are the output of the tree). Nonetheless, similarities abound in the natural world and even more so between the highly related human and non-human primate brains. So, we can begin to study what types of processing in the brain of both humans and monkeys may be similar for communication sounds.
Mapping the Sound Processing and Sound/Visual Integration Areas of the Monkey Brain
We have recently shown that the area of cortex involved in auditory processing is larger than what was once thought (Poremba et al., 2003) and is only slightly smaller in its extent than the visual system. Using the whole-brain mapping method of 2-deoxyglucose utilization we looked at energy use across the brain during the presentation of a wide variety of sounds from pure tones to complex human and monkey vocalizations, music and environmental sounds. In addition to large portions of the parietal, prefrontal, and limbic lobes, the entire superior temporal gyrus is involved in auditory processing of complex sounds and this gyrus encompasses the primary auditory regions known to receive direct auditory information from the thalamus.
This study also delineated areas of overlap between the auditory and visual processing systems allowing us to explore the boundaries of sound only, versus sound plus visual information which is important in our seamless integration of our everyday sensory world. Most of our higher cognitive functions require us to integrate sensory information--for example knowing that an apple is red and round, makes a crunching sound when being eaten and smells heavenly when baked with cinnamon in a pie. Yet we don't know very much about how that process occurs in the brain and having identified these areas and their boundaries in the primate brain that are connected to more than one sensory process (in this case hearing and vision) is a significant step toward understanding how the brain seamlessly integrates the five sensory systems.
Similarities Between the Auditory and Visual Processing Systems
The overall map of the cortical areas involved in sound processing, as well as other recent studies, suggests that it may be organized in a similar manner to the visual system (Poremba et al., 2003; Romanski et al., 1999; Tian & Rauschecker, 2001). The auditory system may be divided into a dorsal stream for object location in space, a ventral stream for object identification, and possibly a third stream for motion processing. Our recent collaborative study in humans requiring identification of human voices versus their location using fMRI has shown a separation of dorsal and ventral auditory processing streams (Rama et al., 2004). Discovering that the auditory system is organized in a similar fashion to the visual system may be helpful since we already know so much about how the brain processes visual information.
Hemispheric Specialization for Monkey Communication Signals
Monkeys have a complex set of vocalizations that can be used to convey a wide variety of information such as food quality, predators, and motivational state (Hauser, 1998; Seyfarth et al., 1980). These communication signals are crucial for survival and reproduction and can be linked to rich conceptual representations. It has been proposed that the vocal calls of monkeys are precursors of human speech, in part because they do provide critical information to other members of the species who rely on them for survival and social interactions (Cheney & Seyfarth, 1990).
Both behavioral and lesion studies suggest that monkeys, like humans, use the auditory system of the left hemisphere preferentially to process vocalizations. Indirect observations of hemispheric specialization for monkey communication signals include preferential head turning to the right when species-specific monkey vocalizations were presented from behind the monkey indicating a left hemisphere processing preference (Ghazanfar & Hauser, 2001). This suggestion is consistent with the study of Heffner and Heffner who made ablations of the auditory cortex on the left and found that those monkeys were impaired in discriminating monkey vocalizations (1984).
Our recent positron emission tomography (PET) imaging study provides for direct observation of hemispheric specialization for monkey communication signals (Poremba et al., 2004). To investigate the pattern of neural activity that might underlie processing of monkey vocalizations, we measured local cerebral metabolic activity by injecting rhesus monkeys with radiolabeled 2-fluoro-2-deoxyglucose (FDG) while the animals listened passively to species-specific calls compared with a variety of other classes of sound including simple and complex non-vocal sounds, phase-scrambled species-specific monkey vocalizations, human speech and ambient background noise. Within the superior temporal gyrus, significantly greater metabolic activity occurred on the left side than on the right, only in the region of the temporal pole and only in response to monkey calls.
When we compared the metabolic activity levels evoked by the different sound classes the hemispheric specialization of the left hemisphere processing may have been induced by suppression across the corpus callosum, the largest fiber tract connecting the two hemispheres. We hypothesized that this trans-commissural suppression of activity in the right temporal pole allowed the left temporal pole to process the species-specific monkey vocalizations. This suppression shuttled across the corpus callosum might be the mechanism underlying the hemispheric lateralization of function. That the corpus callosum can mediate suppression of activity in one hemisphere by activity in another has been demonstrated in the motor system (Ferbert et al., 1992). To test this hypothesis we studied monkeys that had been given commissurotomies (creating split-brain monkeys) in the same way we had tested the intact monkeys. No asymmetry, or hemispheric lateralization, was evident in the temporal poles of the split-brain monkeys; moreover, the activity of the right temporal pole was significantly higher in the split-brain monkeys than in the intact monkeys, thus demonstrating a lack of suppression. These findings support the notion that the mechanism for creating hemispheric lateralization of processing during species-specific monkey vocalizations is suppression of activity in one hemisphere mediated by the corpus callosum.
Two Types of Hemispheric Specialization
Our results suggest that within the monkey's cortical auditory system, two different types of hemispheric lateralization coexist. Although the left temporal pole hemispheric specialization was missing in the split-brain monkeys, there was still a stronger activation in the right hemisphere in many parts of the superior temporal gyrus (STG), i.e., auditory cortex, than on the left. This specialization of hemispheric processing survived the commissurotomy and suggests that there are two types of hemispheric lateralization occurring, one intrahemispherically, and one interhemispherically. The intrahemispheric lateralization, represented in the posterior portion of STG, apparently reflects right-hemisphere specialization for processing a wide variety of acoustic stimulus classes. This specialization seems to be intrinsic to the right hemisphere, in that it is largely independent of concurrent interhemispheric interaction via the forebrain commissures. The other type of lateralization is interhemispheric, mediated by the corpus callosum, and is important in processing the monkey auditory vocal communication sounds represented in the dorsal temporal pole-a late station in the putative ventral auditory pathway-apparently reflects left-hemisphere specialization for processing monkey calls specifically. This interhemispheric type of lateralization depends fully on the forebrain commissures, suggesting that, in the monkey, listening to a brief call can dynamically direct cortical processing to a unilateral substrate specialized for analyzing that call. Whether the left dorsal temporal pole of the monkey is in fact necessary for analyzing species-specific monkey vocalizations will need to be determined with further experiments.
Hemispheric Specialization in Humans, Monkeys, and Lower Animals
Understanding where and how monkeys process auditory communicative signals could help delineate the precursor neural framework for the evolution of language. Because lateralization of language processing is a major cerebral organizing theme in humans, any similar asymmetry in monkeys could reflect an antecedent neural mechanism.
Left-hemisphere specialization for processing of species-specific vocalizations may have an evolutionary origin in nonprimate mammals (Ehret, 1987), paralleling that in birds (George et al., 2002). Monkeys, with their extensive auditory system and large number of distinct vocal communicative signals could provide a useful model approach for uncovering a neural basis for such specialization. Our results open up the possibility of characterizing such neuronal responses in a cortical region of the monkey that is not only a higher-order auditory processing area, but also one that could be a precursor for an acoustic language area in humans.
As mentioned above, hemispheric specialization is not only the domain of primates. Although one might argue in lower animals that many instances are related to the auditory domain. There are other instances of laterality in lower animals outside the auditory system, from chicks and spatial memory, to inhibitory avoidance in rats, and our recent study of amygdala function in a differentially rewarded spatial maze using rats (Vallortigara, 2000; Coleman-Mesches & McGaugh, 1995, Plakke et al., 2004). We must be careful not to assume that lower animals do not have lateralization of function. Often both sides of the brain in lower animals are assumed to accomplish the same task and act in the same manner. Therefore, sometimes values are averaged across hemispheres, only one hemisphere is recorded from, only bilateral lesions are made, or correlations of performance with amount of lesion damage is only made by averaging across hemispheres. This is true of many primate studies as well. It is clear, even from the minimal number of studies listed above, that we cannot lump the left and right hemispheres together and must make some attempt to start separating left from right. We must remain aware that hemispheric specialization is not exclusive to humans nor is it always an exception when it occurs in lower animals.
Special thanks to my collaborators, Mortimer Mishkin, Richard C. Saunders, Megan Malloy, Michelle Cook, Louis Sokoloff, Richard E. Carson, and Peter Herscovitch of the National Institutes of Health, Alison M. Crane of the University of Texas at Austin, Eunjoo Kang, Seoul National University, South Korea, and my students, Emrah Aktunc, Chi Wng Ng, Bethany Plakke, and Maria Imelda Noblejas at the University of Iowa. The intra- and extra-mural programs at the National Institute of Mental Health and the University of Iowa funded this research.
Coleman-Mesches, K., & McGaugh J.L. (1995) Muscimol injected into the right or left amygdaloid complex differentially affects retention performance following aversively motivated training. Brain Res., 676(1),183-188.
Cheney, D.L., & Seyfarth, R.M. (1990) How Monkeys See the World (Univ. Chicago Press, Chicago, IL).
Ehret, G. (1987) Left hemisphere advantage in the mouse brain for recognizing ultrasonic communication calls. Nature, 325, 249-251.
Ferbert, A., et al., (1992) Interhemispheric inhibition of the human motor cortex. J. Physiol;. 453, 525-546.
George, I., Cousillas, H., Richard, J.P., & Hausberger, M. (2002) Song perception in the European starling: Hemispheric specialization and individual variations. C.R. Bio., 325, 197-204.
Ghazanfar, A.A., & Hauser, M.D. (2001) The auditory behavior of primates: a neuroethological perspective. Curr. Opin. Neurobiol. 11, 712-720.
Hauser, M.D. (1998) Functional referents and acoustic similarity: Field playback experiments with rhesys monkeys. Anim. Behav. 55, 1647-1658.
Heffner, H.E., & Heffner, R.S. (1984) Temporal lobe lesions and perception of species-specific vocalizations by macaques. Science 226, 75-76.
Plakke, B., Noblejas, M.I. & Poremba, A. (2004) Lesions of the amygdala impair encoding of differential rewards. Soc. Neurosci. Abstr.
Poremba, A., Malloy, M.M., Saunders, R.C., Carson, R.E., Herscovitch, P., & Mishkin, M. (2004) Species-specific calls evoke asymmetric activity in the monkey's temporal poles. Nature, 427, 448-451.
Poremba, A., Saunders, R.C., Sokoloff, L., Crane, A., Cook, M., & Mishkin, M. (2003) Functional mapping of the primate auditory system. Science, Jan. 2003, 299, 568-572.
Rama, P., Poremba, A., Sala, J.B., Yee, L., Malloy, M., Mishkin, M., & Courtney, S. M. (2004) Dissociable functional cortical topographies for working memory maintenance of voice identity and location. Cerebral Cortex, 14, 768-780.
Romanski, L.M., Tian, B., Fritz, J., Mishkin, M., Goldman-Rakic, P.S., & Rauschecker, J.P. (1999) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci., 12, 1131-1136.
Seyfarth, R.M., Cheney, D.L., & Marler, P. (1980) Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science, 210(4471), 801-803.
Tian, B., Reser, D., Durham, A., Kustov, A., & Rauschecker, J.P. (2001) Functional specialization in rhesus monkey auditory cortex. Science, 292, 290-293.
Vallortiagara, G. (2000) Comparative neuropsychology of the dual brain: A stroll through animals' left and right perceptual worlds. Brain Lang. 73(2), 189-219.
About the Author
Amy Poremba earned her PhD in Psychology from the University of Illinois at Urbana-Champaign in 1996. She is currently an Assistant Professor of Psychology in the Behavioral and Cognitive Neuroscience Area at the University of Iowa and is also a member of the Neuroscience Program. Her research interests focus on the neurobiology of learning and memory at a systems level of analysis, and auditory processing of complex signals. One line of research examines commonalities in the neuronal systems and mechanisms underlying classical, operant, and concept learning in rodents. Another line of research explores the overlap of sensory processing systems and particularly the neural encoding of communication signals in nonhuman primates. Her recent work has mapping the neuronal correlates of general auditory processing and communication signals in rhesus macaques shows some similarities to humans and expands our knowledge about lateralization of brain function.