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Auditory-motor and cognitive aspects in area 8B of macaque monkey’s frontal cortex: a premotor ear–eye field (PEEF)

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Abstract

In previous reports, we showed the involvement of area 8B neurons in both spontaneous ear and eye movement and in auditory information processing. Audition-related cells responded to complex environmental stimuli, but not to pure tones, and their activity changed during visual fixation as a possible inhibitory expression of the engagement of attention. We observed auditory, auditory-motor and motor cells for both eye and ear movements. This finding suggests that area 8B may be involved in the integration of auditory input with ear and eye motor output. In this paper, we extended these previous studies by examining area 8B activity in relation to auditive orienting behaviour, as well as the ocular orientation (i.e., visual fixation) studied previously. Visual fixation led to inhibition of activity in auditory and auditory-motor cells, which suggests that attention may be involved in both, maintaining the eye position and reducing the response of these cell types. Accordingly, during a given task or natural behaviour, spatial attention seems to affect more than one sensorimotor channel simultaneously. These data add to our understanding of how the neural network, through a two-channel attentive process, accomplishes to switch between two effectors, namely eyes and ears. Considering the functional, anatomical and cytoarchitectonic differences among the frontal eye field (FEF), the supplementary eye field (SEF) and area 8B, we propose to consider area 8B as a separate premotor ear–eye field (PEEF).

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References

  • Alain C, Arnott SR, Hevenor S, Graham S, Grady CL (2001) “What” and “Where” in the human auditory system. Proc Natl Acad Sci USA 98:12301–12306

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Mesulam MM (1981) Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J Comp Neurol 200:407–431

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Ghashghaei H, Dombrowski SM, Rempel-Clower NL (1999) Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J Comp Neurol 410:343–367

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Medalla M, Alade O, Suski J, Zikopoulos B, Lera P (2005) Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey. Cereb Cortex 15:1356–1370

    Article  PubMed  CAS  Google Scholar 

  • Bell AH, Corneil BD, Munoz DP, Meredith MA (2003) Engagement of visual fixation suppresses sensory responsiveness and multisensory integration in the primate superior colliculus. Eur J Neurosci 18:2867–2873

    Article  PubMed  CAS  Google Scholar 

  • Bon L, Lucchetti C (1991) Behavioural and motor mechanisms of dorsomedial frontal cortex of macaca monkey. Int J Neurosci 60:187–193

    Article  PubMed  CAS  Google Scholar 

  • Bon L, Lucchetti C (1992) The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity. Exp Brain Res 89:571–580

    Article  PubMed  CAS  Google Scholar 

  • Bon L, Lucchetti C (1994) Ear and eye representation in the frontal cortex, area 8b, of the macaque monkey: an electrophysiological study. Exp Brain Res 102:259–271

    Article  PubMed  CAS  Google Scholar 

  • Bon L, Lucchetti C (1997) Attentional-related neurons in the supplementary eye field of the macaque monkey. Exp Brain Res 113:180–185

    Article  PubMed  CAS  Google Scholar 

  • Bon L, Lucchetti C (2006) Auditory environmental cells and visual fixation effect in area 8B of macaque monkey. Exp Brain Res 168:441–449

    Article  PubMed  Google Scholar 

  • Bruce CJ, Goldberg ME, Bushnell MC, Stanton GB (1985) Primate frontal eye fields: II. Physiological and anatomic correlates of electrically evoked eye movements. J Neurophysiol 54:714–734

    PubMed  CAS  Google Scholar 

  • Chen LL, Walton MMG (2005) Head movement evoked by electric stimulation in the supplementary eye field of the rhesus monkey. J Neurophysiol 94:4502–4519

    Article  PubMed  Google Scholar 

  • Cherry EC (1953) Some experiments on the recognition of speech with one and with two ears. J Acust Soc Am 25:975–979

    Article  Google Scholar 

  • Cohen YE, Russ BE, Gifford III GW (2005) Auditory processing in the posterior parietal cortex. Behav Cogn Neurosci Rev 4:218–231

    Article  PubMed  Google Scholar 

  • Fries W (1984) Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230:55–76

    Article  PubMed  CAS  Google Scholar 

  • Fuster JM, Bodner M, Kroger JK (2000) Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405:347–351

    Article  PubMed  CAS  Google Scholar 

  • Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK (2005) Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J Neurosci 18:5004–5012

    Article  Google Scholar 

  • Gifford III GW, Cohen YE (2004) The effect of a central fixation light on auditory spatial responses in area LIP. J Neurophysiol 91:2929–2933

    Article  PubMed  Google Scholar 

  • Jay MF, Sparks DL (1987) Sensorimotor integration in the superior colliculus. II. Coordinates of auditory signals. J Neurophysiol 57:35–55

    PubMed  CAS  Google Scholar 

  • Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coil for measurement of eye position: an improved method. Vision Res 20:535–538

    Article  PubMed  CAS  Google Scholar 

  • Kaas JH, Hackett TA (2000) Subdivision of auditory cortex and processing streams in primates. Proc Natl Acad Sci USA 97:11793–11799

    Article  PubMed  CAS  Google Scholar 

  • Kass RE, Ventura V, Brown EN (2005) Statistical Issue in the analysis of neuronal data. J Neurophysiol 94:8–25

    Article  PubMed  Google Scholar 

  • Levinsohn G (1909) Uber die beziehungen der grosshirnrinde beim affen zu den bewegungen des auges. Graefes Arch Clin Exp Ophthalmol 71:313–378

    Google Scholar 

  • Lucchetti C, Lui F, Bon L (1998) Neglect syndrome for aversive stimuli in a macaque monkey with dorsomedial frontal cortex lesion. Neuropsychologia 36:251–257

    Article  PubMed  CAS  Google Scholar 

  • Luppino G, Rozzi S, Calzavara R, Matelli M (2003) Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur J Neurosci 17:559–578

    Article  PubMed  Google Scholar 

  • Lynch JC, Hoover JE, Strick PL (1994) Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp Brain Res 100:181–186

    Article  PubMed  CAS  Google Scholar 

  • Mann SE, Thau R, Schiller PH (1988) Conditional task-related responses in monkey dorsomedial frontal cortex. Exp Brain Res 69:460–468

    Article  PubMed  CAS  Google Scholar 

  • Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311:445–462

    Article  PubMed  CAS  Google Scholar 

  • Middleton FA, Strick PL (2001) Cerebellar projections to the prefrontal cortex of the primate. J Neurosci 21:700–712

    PubMed  CAS  Google Scholar 

  • Mitz AR, Godschalk M (1989) Eye-movement representation in the frontal lobe of rhesus monkeys. Neurosci Lett 106:157–162

    Article  PubMed  CAS  Google Scholar 

  • Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W, Guldin W, Hadjidimitrakis K, Savaki HE (2004) Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14 C]-2-deoxyglucose functional imaging study. J Neurosci 24:5726–5740

    Article  PubMed  CAS  Google Scholar 

  • Pandya DN, Yeterian EH (1985) Architecture and connections of cortical association areas. In: Peters A, Jones EG (eds) Association and auditory cortices. Plenum, New York, pp 3–61

    Google Scholar 

  • Passingham R (1993) In: The frontal lobes and voluntary action. Oxford Psychology Series NO 21

  • Petrides M, Pandya DN (1994) Comparative architectonic analysis of the human and the macaque frontal cortex. In: Boller F, Grafman J (eds) Handbook of neuropsychology, vol 9. Elsevier, Amsterdam, pp 17–57

    Google Scholar 

  • Populin LC, Yin TCT (1998) Pinna movements of the cat during sound localization. J Neuroscience 18:4233–4243

    CAS  Google Scholar 

  • Populin LC, Yin TCT (2002) Bimodal interactions in the superior colliculus of the behaving cat. J Neurosci 22:2826–2834

    PubMed  CAS  Google Scholar 

  • Preuss TM, Stepniewska I, Kaas JH (1996) Movement representation in the dorsal and ventral premotor areas of Owl monkeys: a microstimulation study. J Comp Neurol 371:649–676

    Article  PubMed  CAS  Google Scholar 

  • Rao SC, Rainer G, Miller EK (1997) Integration of what and where in the primate prefrontal cortex. Science 276:821–824

    Article  PubMed  CAS  Google Scholar 

  • Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds in the macaque non primary auditory cortex. Science 268:111–114

    Article  PubMed  CAS  Google Scholar 

  • Recanzone GH (2000) Spatial processing in the auditory cortex of the macaque monkey. Proc Natl Acad Sci USA 97:11829–11835

    Article  PubMed  CAS  Google Scholar 

  • Remmel RS (1984) An inexpensive eye movement monitor using the scleral coil technique. IEEE Trans Biomed Engin BME 31(4):388–390

    Article  CAS  Google Scholar 

  • Rizzolatti G, Craighero L (1998) Spatial attention: mechanisms and theories. In: Sabourin M, Craik F, Robert M (eds) Advances in psychological science: biological and cognitive aspects, vol 2. Psychological Press, Francis & Taylor, pp 171–198

    Google Scholar 

  • Rizzolatti G, Camarda R, Grupp LA, Pisa M (1974) Inhibitory effect of remote visual stimuli on visual responses of cat superior colliculus: spatial and temporal factors. J Neurophysiol 37:1262–1275

    PubMed  CAS  Google Scholar 

  • Romanski LM, Bates JF, Goldman-Rakic PS (1999) Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 403:141–157

    Article  PubMed  CAS  Google Scholar 

  • Russo GS, Bruce CJ (1994) Frontal eye field activity preceding aurally guided saccades. J Neurophysiol 71:1250–1253

    PubMed  CAS  Google Scholar 

  • Schall JD (1991) Neuronal activity related to visually guided saccadic eye-movements in the supplementary motor area of Rhesus monkeys J. Neurophysiology 66:530–558

    PubMed  CAS  Google Scholar 

  • Schall JD (1997) Visuomotor areas of the frontal lobe in cerebral cortex. In: Rockland KS, Kaas JH, Peters A (eds) Extrastriate cortex in primates, vol 12. Plenum Press, New York, pp. 527–616

    Google Scholar 

  • Schlag J, Schlag-Rey M (1987) Evidence for a supplementary eye field. J Neurophysiol 57:179–200

    PubMed  CAS  Google Scholar 

  • Schmahmann JD, Pandya DN (1997) Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci 17:438–458

    PubMed  CAS  Google Scholar 

  • Stepniewska I, Preuss TM, Kaas JH (1993) Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J Comp Neurol 330:238–271

    Article  PubMed  CAS  Google Scholar 

  • Tanila H, Carlson S, Linnankoski I, Lindros F, Kahila H (1992) Functional properties of dorsolateral prefrontal cortical neurons in awake monkey. Behav Brain Res 47:169–180

    Article  PubMed  CAS  Google Scholar 

  • Tanila H, Carlson S, Linnankoski I, Kahila H (1993) Regional distribution of functions in dorsolateral prefrontal cortex of the monkey. Behav Brain Res 53:63–71

    Article  PubMed  CAS  Google Scholar 

  • Tehovnik EJ, Lee KM (1993) The dorsomedial frontal cortex of the rhesus monkey. Topographic representation of saccades evoked by electric stimulation. Exp Brain Res 96:430–442

    Article  PubMed  CAS  Google Scholar 

  • Tehovnik EJ, Sommer MS (1997) Electrically evoked saccades from the dorsomedial frontal cortex and frontal eye field: a parametric evaluation reveals differences between areas. Exp Brain Res 117:369–378

    Article  PubMed  CAS  Google Scholar 

  • Tehovnik EJ, Sommer MA, Chou IH, Slocum WM, Schiller PH (2000) Eye fields in the frontal lobes of primates. Brain Res Rev 32:413–448

    Article  PubMed  CAS  Google Scholar 

  • Turatto M, Galfano G, Bridgeman B, Umiltà C (2004) Space-independent modality-driven attentional capture in auditory, tactile and visual systems. Exp Brain Res 155:301–310

    Article  PubMed  Google Scholar 

  • Vaadia E, Benson DA, Hienz RD, Goldstein MH (1986) Unit study of monkey frontal cortex: active localization of auditory and of visual stimuli. J Neurophysiol 56:934–952

    PubMed  CAS  Google Scholar 

  • Von Bonin G, Bailey P (1947) The neocortex of macaca mulatta. University of Illinois Press, Urbana

    Google Scholar 

  • Walker AE (1940) A cytoarchitectural study of frontal area of the macaque monkey. J Comp Neurol 73:59–86

    Article  Google Scholar 

  • Wang YW, Isoda M, Matsuzaka Y, Shima K, Tanji J (2005) Prefrontal cortical cells projecting to the supplementary eye field and presupplementary motor area in the monkey. Neurosci Res 53:1–7

    Article  PubMed  Google Scholar 

  • Wessinger CM, Van Meter J, Tian B, Van Lare J, Pekar J, Rauschecker JP (2001) Hierarchical organization of the human auditory cortex revealed by functional magnetic resonance imaging. J Cogn Neurosci 13:1–7

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We wish to thank Dr. Steven Wise for English revision, Dr. Marcello Manfredi for volume measurements, Prof. Rodolfo Cecchi prorector University of Modena and Reggio-Emilia for his support for this type of research and for improvements in animal housing, Dr. Vasco Lolli and Mr. Vincenzo Molino for animal care. Grants were provided by University of Modena and Reggio Emilia, Foundation Cassa di Risparmio of Modena and PRIN 2005.

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Lucchetti, C., Lanzilotto, M. & Bon, L. Auditory-motor and cognitive aspects in area 8B of macaque monkey’s frontal cortex: a premotor ear–eye field (PEEF). Exp Brain Res 186, 131–141 (2008). https://doi.org/10.1007/s00221-007-1216-5

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