Abstract
Language and communication rely on the combination of visual and auditory information. The frontal lobes have long been known to support communication processing and receive a wide array of sensory inputs from many brain regions. The ventral frontal lobe, specifically the ventrolateral prefrontal cortex (VLPFC), receives afferents from auditory and visual association cortices. Recordings in nonhuman primates indicate that single neurons in the VLPFC integrate face and vocal stimuli. These multisensory neurons show enhanced and suppressed responses to face and vocalization combinations. Furthermore, studies indicate that ventral prefrontal neurons are affected by the semantic congruence of face-vocalization pairs and by the temporal synchrony of dynamic face-vocalization stimuli. Recordings of VLPFC neurons in macaques performing working memory tasks demonstrate that neurons are context dependent and respond to specific combinations of face and vocal stimuli during memory and decision tasks. Finally, transient inactivation of the prefrontal cortex impairs working memory for face-vocalization stimuli. Thus, results from several studies indicate that the primate prefrontal cortex plays an important role in the processing and integration of face and vocalization information that is essential during communication and social cognition.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Adachi, I., & Hampton, R. (2011). Rhesus monkeys see who they hear: Spontaneous cross-modal memory for familiar conspecifics. PLoS One, 6(8), e23345.
Asaad, W. F., Rainer, G., & Miller, E. K. (2000). Task-specific neural activity in the primate prefrontal cortex. Journal of Neurophysiology, 84, 451–459.
Averbeck, B. B., & Romanski, L. M. (2006). Probabilistic encoding of vocalizations in macaque ventral lateral prefrontal cortex. The Journal of Neuroscience, 26, 11023–11033.
Barbas, H. (1992). Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. Advances in Neurology, 57, 91–115.
Barraclough, N. E., Xiao, D., Baker, C. I., Oram, M. W., & Perrett, D. I. (2005). Integration of visual and auditory information by superior temporal sulcus neurons responsive to the sight of actions. Journal of Cognitive Neuroscience, 17(3), 377–391.
Baum, S. H., Stevenson, R. A., & Wallace, M. T. (2015). Behavioral, perceptual, and neural alterations in sensory and multisensory function in autism spectrum disorder. Progress in Neurobiology, 134, 140–160.
Baxter, M. G., Gaffan, D., Kyriazis, D. A., & Mitchell, A. S. (2009). Ventrolateral prefrontal cortex is required for performance of a strategy implementation task but not reinforcer devaluation effects in rhesus monkeys. European Journal of Neuroscience, 29(10), 2049–2059.
Bodner, M., Kroger, J., & Fuster, J. M. (1996). Auditory memory cells in dorsolateral prefrontal cortex. Neuroreport, 7, 1905–1908.
Brody, C. D., Hernandez, A., Zainos, A., & Romo, R. (2003). Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cerebral Cortex, 13(11), 1196–1207.
Bussey, T. J., Wise, S. P., & Murray, E. A. (2002). Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. Behavioral Neuroscience, 116(4), 703–715.
Cohen, Y. E., Russ, B. E., Davis, S. J., Baker, A. E., Ackelson, A. L., & Nitecki, R. (2009). A functional role for the ventrolateral prefrontal cortex in non-spatial auditory cognition. Proceedings of the National Academy of Sciences of the United States of America, 106(47), 20045–20050.
Crottaz-Herbette, S., Anagnoson, R. T., & Menon, V. (2004). Modality effects in verbal working memory: Differential prefrontal and parietal responses to auditory and visual stimuli. NeuroImage, 21(1), 340–351.
Diehl, M. M., & Romanski, L. M. (2014). Responses of prefrontal multisensory neurons to mismatching faces and vocalizations. The Journal of Neuroscience, 34(34), 11233–11243.
Eliades, S. J., & Wang, X. (2012). Neural correlates of the Lombard effect in primate auditory cortex. The Journal of Neuroscience, 32(31), 10737–10748.
Fuster, J. M., Bodner, M., & Kroger, J. K. (2000). Cross-modal and cross-temporal association in neurons of frontal cortex. Nature, 405(6784), 347–351.
Ghazanfar, A. A., Maier, J. X., Hoffman, K. L., & Logothetis, N. K. (2005). Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. The Journal of Neuroscience, 25(20), 5004–5012.
Ghazanfar, A. A., Morrill, R. J., & Kayser, C. (2013). Monkeys are perceptually tuned to facial expressions that exhibit a theta-like speech rhythm. Proceedings of the National Academy of Sciences of the United States of America, 110(5), 1959–1963.
Gifford, G. W., III, Maclean, K. A., Hauser, M. D., & Cohen, Y. E. (2005). The neurophysiology of functionally meaningful categories: Macaque ventrolateral prefrontal cortex plays a critical role in spontaneous categorization of species-specific vocalizations. Journal of Cognitive Neuroscience, 17, 1471–1482.
Goldman-Rakic, P. S. (1987). Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In F. Plum (Ed.), Handbook of physiology, Vol. V: Higher functions of the brain: The nervous system, Sect. 1 (pp. 373–418). Bethesda: American Physiological Society.
Gross, C. G., & Weiskrantz, L. (1962). Evidence for dissociation of impairment on auditory discrimination and delayed response following lateral frontal lesions in monkeys. Experimental Neurology, 5, 453–476.
Habbershon, H. M., Ahmed, S. Z., & Cohen, Y. E. (2013). Rhesus macaques recognize unique multimodal face-voice relations of familiar individuals and not of unfamiliar ones. Brain, Behavior and Evolution, 81(4), 219–225.
Hackett, T. A., Stepniewska, I., & Kaas, J. H. (1998). Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. Journal of Comparative Neurology, 394, 475–495.
Hackett, T. A., Stepniewska, I., & Kaas, J. H. (1999). Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Research, 817, 45–58.
Hackett, T. A., de la Mothe, L. A., Camalier, C. R., Falchier, A., Lakatos, P., Kajikawa, Y., & Schroeder, C. E. (2014). Feedforward and feedback projections of caudal belt and parabelt areas of auditory cortex: Refining the hierarchical model. Frontiers in Neuroscience, 8, 72.
Hage, S. R., & Nieder, A. (2013). Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations. Nature Communications, 4, 2409.
Hage, S. R., & Nieder, A. (2015). Audio-vocal interaction in single neurons of the monkey ventrolateral prefrontal cortex. The Journal of Neuroscience, 35, 7030–7040.
Hershenson, M. (1962). Reaction time as a measure of intersensory facilitation. Journal of Experimental Psychology, 63, 289–293.
Hwang, J., & Romanski, L. M. (2015). Prefrontal neuronal responses during audiovisual nmemonic processing. The Journal of Neuroscience, 35, 960–971.
Iversen, S. D., & Mishkin, M. (1973). Comparison of superior temporal and inferior prefrontal lesions on auditory and non-auditory tasks in rhesus monkeys. Brain Research, 55(2), 355–367.
Jones, E. G., Dell’Anna, M. E., Molinari, M., Rausell, E., & Hashikawa, T. (1995). Subdivisions of macaque monkey auditory cortex revealed by calcium-binding protein immunoreactivity. Journal of Comparative Neurology, 362, 153–170.
Jurgens, U. (2009). The neural control of vocalization in mammals: A review. Journal of Voice, 23(1), 1–10.
Kosaki, H., Hashikawa, T., He, J., & Jones, E. G. (1997). Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys. Journal of Comparative Neurology, 386(2), 304–316.
Laurienti, P. J., Wallace, M. T., Maldjian, J. A., Susi, C. M., Stein, B. E., & Burdette, J. H. (2003). Cross-modal sensory processing in the anterior cingulate and medial prefrontal cortices. Human Brain Mapping, 19(4), 213–223.
McGurk, H., & MacDonald, J. (1976). Hearing lips and seeing voices. Nature, 264, 746–748.
Medalla, M., & Barbas, H. (2014). Specialized prefrontal “auditory fields”: Organization of primate prefrontal-temporal pathways. Frontiers in Neuroscience, 8, 77.
Meredith, M. A., & Stein, B. E. (1986). Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. Journal of Neurophysiology, 56(3), 640–662.
Miller, L. M., & D’Esposito, M. (2005). Perceptual fusion and stimulus coincidence in the cross-modal integration of speech. The Journal of Neuroscience, 25, 5884–5893.
Miller, E. K., Li, L., & Desimone, R. (1991). A neural mechanism for working and recognition memory in inferior temporal cortex. Science, 254(5036), 1377–1379.
Miller, E. K., Erickson, C. A., & Desimone, R. (1996). Neural mechanisms of visual working memory in prefrontal cortex of the macaque. The Journal of Neuroscience, 16, 5154–5167.
Mishkin, M., & Manning, F. J. (1978). Non-spatial memory after selective prefrontal lesions in monkeys. Brain Research, 143, 313–323.
Molholm, S., Ritter, W., Javitt, D. C., & Foxe, J. J. (2004). Multisensory visual-auditory object recognition in humans: A high-density electrical mapping study. Cerebral Cortex, 14(4), 452–465.
O’Scalaidhe, S. P., Wilson, F. A., & Goldman-Rakic, P. S. (1997). Areal segregation of face-processing neurons in prefrontal cortex. Science, 278, 1135–1138.
O’Scalaidhe, S. P. O., Wilson, F. A. W., & Goldman-Rakic, P. G. R. (1999). Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: Evidence for intrinsic specialization of neuronal coding. Cerebral Cortex, 9, 459–475.
Passingham, R. (1975). Delayed matching after selective prefrontal lesions in monkeys (Macaca mulatta). Brain Research, 92, 89–102.
Passingham, R. E., Toni, I., & Rushworth, M. F. (2000). Specialisation within the prefrontal cortex: The ventral prefrontal cortex and associative learning. Experimental Brain Research, 133(1), 103–113.
Petrides, M., & Pandya, D. N. (2002). Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. European Journal of Neuroscience, 16(2), 291–310.
Plakke, B., & Romanski, L. M. (2014). Auditory connections and functions of prefrontal cortex. Frontiers in Neuroscience, 8, 199.
Plakke, B., Diltz, M. D., & Romanski, L. M. (2013a). Coding of vocalizations by single neurons in ventrolateral prefrontal cortex. Hearing Research, 305, 135–143.
Plakke, B., Ng, C. W., & Poremba, A. (2013b). Neural correlates of auditory recognition memory in primate lateral prefrontal cortex. Neuroscience, 244, 62–76.
Plakke, B., Hwang, J., & Romanski, L. M. (2015). Inactivation of primate prefrontal cortex impairs auditory and audiovisual working memory. The Journal of Neuroscience, 35, 9666–9675.
Posner, M. I., Nissen, M. J., & Klein, R. M. (1976). Visual dominance: An information-processing account of its origins and significance. Psychological Review, 83(2), 157–171.
Price, C. J. (2012). A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. NeuroImage, 62(2), 816–847.
Rama, P., & Courtney, S. M. (2005). Functional topography of working memory for face or voice identity. NeuroImage, 24(1), 224–234.
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.
Rauschecker, J. P., Tian, B., & Hauser, M. (1995). Processing of complex sounds in the macaque nonprimary auditory cortex. Science, 268(5207), 111–114.
Romanski, L. M. (2012). Integration of faces and vocalizations in ventral prefrontal cortex: Implications for the evolution of audiovisual speech. Proceedings of the National Academy of Sciences of the United States of America, 109(Suppl 1), 10717–10724.
Romanski, L. M., & Averbeck, B. B. (2009). The primate cortical auditory system and neural representation of conspecific vocalizations. Annual Review of Neuroscience, 32, 315–346.
Romanski, L. M., & Diehl, M. M. (2011). Neurons responsive to face-view in the primate ventrolateral prefrontal cortex. Neuroscience, 189, 223–235.
Romanski, L. M., & Goldman-Rakic, P. S. (2002). An auditory domain in primate prefrontal cortex. Nature Neuroscience, 5, 15–16.
Romanski, L. M., & Hwang, J. (2012). Timing of audiovisual inputs to the prefrontal cortex and multisensory integration. Neuroscience, 214, 36–48.
Romanski, L. M., Bates, J. F., & Goldman-Rakic, P. S. (1999a). Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. Journal of Comparative Neurology, 403, 141–157.
Romanski, L. M., Tian, B., Fritz, J., Mishkin, M., Goldman-Rakic, P. S., & Rauschecker, J. P. (1999b). Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nature Neuroscience, 2(12), 1131–1136.
Romanski, L. M., Averbeck, B. B., & Diltz, M. (2005). Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. Journal of Neurophysiology, 93(2), 734–747.
Rushworth, M. F., Nixon, P. D., Eacott, M. J., & Passingham, R. E. (1997). Ventral prefrontal cortex is not essential for working memory. The Journal of Neuroscience, 17(12), 4829–4838.
Russ, B. E., Orr, L. E., & Cohen, Y. E. (2008). Prefrontal neurons predict choices during an auditory same-different task. Current Biology, 18(19), 1483–1488.
Rygula, R., Walker, S. C., Clarke, H. F., Robbins, T. W., & Roberts, A. C. (2010). Differential contributions of the primate ventrolateral prefrontal and orbitofrontal cortex to serial reversal learning. The Journal of Neuroscience, 30(43), 14552–14559.
Schumacher, E. H., Lauber, E., Awh, E., Jonides, J., Smith, E. E., & Koeppe, R. A. (1996). PET evidence for an amodal verbal working memory system. NeuroImage, 3(2), 79–88.
Strand, F., Forssberg, H., Klingberg, T., & Norrelgen, F. (2008). Phonological working memory with auditory presentation of pseudo-words—An event related fMRI study. Brain Research, 1212, 48–54.
Sugihara, T., Diltz, M. D., Averbeck, B. B., & Romanski, L. M. (2006). Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex. The Journal of Neuroscience, 26, 11138–11147.
Tanila, H., Carlson, S., Linnankoski, I., Lindroos, F., & Kahila, H. (1992). Functional properties of dorsolateral prefrontal cortical neurons in awake monkey. Behavioral Brain Research, 47, 169–180.
Tanila, H., Carlson, S., Linnankoski, I., & Kahila, H. (1993). Regional distribution of functions in dorsolateral prefrontal cortex of the monkey. Behavioral Brain Research, 53, 63–71.
Vaadia, E., Benson, D. A., Hienz, R. D., & Goldstein, M. H., Jr. (1986). Unit study of monkey frontal cortex: Active localization of auditory and of visual stimuli. Journal of Neurophysiology, 56, 934–952.
Watson, R., Latinus, M., Noguchi, T., Garrod, O., Crabbe, F., & Belin, P. (2013). Dissociating task difficulty from incongruence in face-voice emotion integration. Frontiers in Human Neuroscience, 7, 744.
West, R. A., & Larson, C. R. (1995). Neurons of the anterior mesial cortex related to faciovocal activity in the awake monkey. Journal of Neurophysiology, 74(5), 1856–1869.
Wilson, F. A., O’Scalaidhe, S. P., & Goldman-Rakic, P. S. (1993). Dissociation of object and spatial processing domains in primate prefrontal cortex. Science, 260, 1955–1958.
Yu, J. C., Chang, T. Y., & Yang, C. T. (2014). Individual differences in working memory capacity and workload capacity. Frontiers in Psychology, 5, 1465.
Acknowledgments
The authors acknowledge the hard work and assistance of Theodore Lincoln and Skye Kevelson in writing, editing, and figure creation. We also thank Adrian K. C. Lee, Mark Wallace, Allison Coffin, and Arthur N. Popper for all their helpful comments and suggestions in editing this chapter.
Compliance with Ethics Requirements
Lizabeth M. Romanski declares that she has no conflict of interest.
Bethany Plakke declares that she has no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Plakke, B., Romanski, L.M. (2019). Audiovisual Integration in the Primate Prefrontal Cortex. In: Lee, A., Wallace, M., Coffin, A., Popper, A., Fay, R. (eds) Multisensory Processes. Springer Handbook of Auditory Research, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-10461-0_7
Download citation
DOI: https://doi.org/10.1007/978-3-030-10461-0_7
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-10459-7
Online ISBN: 978-3-030-10461-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)