Integration of Auditory and Visual Communication Information in the Primate Ventrolateral Prefrontal Cortex

The integration of auditory and visual stimuli is crucial for recognizing objects, communicating effectively, and navigating through our complex world. Although the frontal lobes are involved in memory, communication, and language, there has been no evidence that the integration of communication information occurs at the single-cell level in the frontal lobes. Here, we show that neurons in the macaque ventrolateral prefrontal cortex (VLPFC) integrate audiovisual communication stimuli. The multisensory interactions included both enhancement and suppression of a predominantly auditory or a predominantly visual response, although multisensory suppression was the more common mode of response. The multisensory neurons were distributed across the VLPFC and within previously identified unimodal auditory and visual regions (O'Scalaidhe et al., 1997; Romanski and Goldman-Rakic, 2002). Thus, our study demonstrates, for the first time, that single prefrontal neurons integrate communication information from the auditory and visual domains, suggesting that these neurons are an important node in the cortical network responsible for communication.

[1]  Joost X. Maier,et al.  Multisensory Integration of Dynamic Faces and Voices in Rhesus Monkey Auditory Cortex , 2005 .

[2]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[4]  S. Kojima,et al.  Matching vocalizations to vocalizing faces in a chimpanzee (Pan troglodytes) , 2004, Animal Cognition.

[5]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Apostolos P. Georgopoulos,et al.  Neural activity in prefrontal cortex during copying geometrical shapes , 2003, Experimental Brain Research.

[7]  G. Westergaard,et al.  Auditory--visual cross-modal perception of communicative stimuli in tufted capuchin monkeys (Cebus apella). , 2005, Journal of experimental psychology. Animal behavior processes.

[8]  B. Stein,et al.  Interactions among converging sensory inputs in the superior colliculus. , 1983, Science.

[9]  G. Calvert.  Crossmodal processing in the human brain: insights from functional neuroimaging studies. , 2001, Cerebral cortex.

[10]  P. Marler,et al.  The role of articulation in the production of rhesus monkey, Macaca mulatta, vocalizations , 1993, Animal Behaviour.

[11]  Paul J. Laurienti,et al.  On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies , 2005, Experimental Brain Research.

[12]  E. Miller,et al.  THE PREFRONTAL CORTEX AND COGNITIVE CONTROL , 2000 .

[13]  P. Marler,et al.  Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors , 1993 .

[14]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[15]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[16]  Chris I. Baker,et al.  Integration of Visual and Auditory Information by Superior Temporal Sulcus Neurons Responsive to the Sight of Actions , 2005, Journal of Cognitive Neuroscience.

[17]  J. Ringo.  Stimulus specific adaptation in inferior temporal and medial temporal cortex of the monkey , 1996, Behavioural Brain Research.

[18]  H. McGurk,et al.  Hearing lips and seeing voices , 1976, Nature.

[19]  P S Goldman-Rakic,et al.  Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. , 1999, Cerebral cortex.

[20]  D. Pandya,et al.  Frontal lobe connections of the superior temporal sulcus in the rhesus monkey , 1989, The Journal of comparative neurology.

[21]  J. Armony,et al.  Sensitivity to voice in human prefrontal cortex. , 2005, Journal of neurophysiology.

[22]  P. Goldman-Rakic,et al.  Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey , 1999, The Journal of comparative neurology.

[23]  C. Rosenkilde,et al.  Functional heterogeneity of the prefrontal cortex in the monkey: a review. , 1979, Behavioral and neural biology.

[24]  T. Stanford,et al.  Evaluating the Operations Underlying Multisensory Integration in the Cat Superior Colliculus , 2005, The Journal of Neuroscience.

[25]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

[26]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[27]  Mikko Sams,et al.  Processing of audiovisual speech in Broca's area , 2005, NeuroImage.

[28]  B. Stein,et al.  Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  C. Price.  The functional anatomy of word comprehension and production , 1998, Trends in Cognitive Sciences.

[30]  Marc D. Hauser,et al.  The Neurophysiology of Functionally Meaningful Categories: Macaque Ventrolateral Prefrontal Cortex Plays a Critical Role in Spontaneous Categorization of Species-Specific Vocalizations , 2005, Journal of Cognitive Neuroscience.

[31]  Jeffery A. Jones,et al.  Brain activity during audiovisual speech perception: An fMRI study of the McGurk effect , 2003, Neuroreport.

[32]  S. Iversen,et al.  Detection of Audio-Visual Integration Sites in Humans by Application of Electrophysiological Criteria to the BOLD Effect , 2001, NeuroImage.

[33]  B. Seltzer,et al.  Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex , 1995, The Journal of comparative neurology.

[34]  Sidney S. Simon,et al.  Merging of the Senses , 2008, Front. Neurosci..

[35]  J. Fuster.  The Prefrontal Cortex , 1997 .

[36]  N. Logothetis,et al.  Neuroperception: Facial expressions linked to monkey calls , 2003, Nature.

[37]  Yasushi Miyashita,et al.  From Perception to Sentence Comprehension: The Convergence of Auditory and Visual Information of Language in the Left Inferior Frontal Cortex , 2002, NeuroImage.

[38]  James K. Kroger,et al.  Cross-modal and cross-temporal association in neurons of frontal cortex , 2000, Nature.

[39]  B. Stein,et al.  Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. , 1986, Journal of neurophysiology.

[40]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[41]  E. Pucci,et al.  Percutaneous ethanol injection therapy of autonomous nodule and amiodarone-induced thyrotoxicosis. , 1994, Thyroidology.

[42]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[43]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[44]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[45]  J M Fuster,et al.  Auditory memory cells in dorsolateral prefrontal cortex. , 1996, Neuroreport.

[46]  L. Benevento,et al.  Auditory-visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey , 1977, Experimental Neurology.

[47]  Lee M. Miller,et al.  Behavioral/systems/cognitive Perceptual Fusion and Stimulus Coincidence in the Cross- Modal Integration of Speech , 2022 .

[48]  Giacomo Rizzolatti,et al.  Neurons responding to visual stimuli in the frontal lobe of macaque monkeys , 1979, Neuroscience Letters.

[49]  A. Georgopoulos,et al.  Neural activity in prefrontal cortex during copying geometrical shapes , 2003, Experimental brain research.

[50]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[51]  J. Kaas,et al.  Prefrontal connections of the parabelt auditory cortex in macaque monkeys , 1999, Brain Research.

[52]  P. Goldman-Rakic,et al.  Areal segregation of face-processing neurons in prefrontal cortex. , 1997, Science.

[53]  G. Calvert,et al.  Multisensory integration: methodological approaches and emerging principles in the human brain , 2004, Journal of Physiology-Paris.

[54]  Charles E. Heckler,et al.  Applied Multivariate Statistical Analysis , 2005, Technometrics.

[55]  H. Spinnler.  The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

[56]  D. Pandya,et al.  Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey , 1988, The Journal of comparative neurology.

[57]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

[58]  Bruno B Averbeck,et al.  Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. , 2005, Journal of neurophysiology.

[59]  P. Goldman-Rakic,et al.  Myelo‐ and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[60]  H. Barbas,et al.  Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. , 1992, Advances in neurology.

[61]  P. Goldman-Rakic,et al.  An auditory domain in primate prefrontal cortex , 2002, Nature Neuroscience.

[62]  D. Gaffan,et al.  Auditory-visual associations, hemispheric specialization and temporal-frontal interaction in the rhesus monkey. , 1991, Brain : a journal of neurology.