Cerebral Cortex, Vol. 9, No. 5, 459-475,
July 1999
© 1999 Oxford University Press
Face-selective Neurons During Passive Viewing and Working Memory Performance of Rhesus Monkeys: Evidence for Intrinsic Specialization of Neuronal Coding
Section of Neurobiology, Yale University Medical School, New Haven, CT 06510, USA
The functional organization of prefrontal cortex (PFC) is a central issue in cognitive neuroscience. Previous physiological investigations have often failed to reveal specialization within the PFC. However, these studies have generally not been designed to examine this issue. Methodological issues such as statistical criteria for specificity, the number of neurons sampled, the extent of cortex sampled, and the number, location and nature of the stimuli used are among the variables that need to be considered in evaluating the results of studies on functional localization. In the present study, we have examined neurons in macaque monkeys trained to fixate while viewing visual stimuli, including faces, or to use them as memoranda on a working memory task. Visual responses of over 1500 neurons were recorded throughout a wide expanse of the PFC (areas 12, 9, 46, 8 and 45). Neurons were considered selective for faces if the best response to a face was over twice as strong as that to any of a wide variety of non-face stimuli. Full electrode track reconstructions in three monkeys revealed in each that neurons which met this criterion were concentrated almost exclusively in three distinct subregions within the projection region of the temporal lobe visual areas. We further show that for all neurons, the most visually selective neurons (for faces, objects or color patterns) were also the most concentrated in the temporal lobe recipient PFC. Similar face selectivity, regional specialization, and delay or delay-like activity were observed in monkeys whether trained on memory tasks or not, which suggests that these are naturally occurring properties of prefrontal neurons. These results confirm neuronal and regional specialization for information processing in PFC and elucidate how heretofore unexamined experimental variables have a strong influence on the detection of regional specialization.
1 Current address: ARL Division of Neural Systems, University of Arizona, Life Sciences North Building, Tuscon, AZ 85724, USA
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  B. B. Averbeck, A. Battaglia-Mayer, C. Guglielmo, and R. Caminiti Statistical Analysis of Parieto-Frontal Cognitive-Motor Networks J Neurophysiol, September 1, 2009; 102(3): 1911 - 1920. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Borra, N. Ichinohe, T. Sato, M. Tanifuji, and K. S. Rockland Cortical Connections to Area TE in Monkey: Hybrid Modular and Distributed Organization Cereb Cortex, May 23, 2009; (2009) bhp096v2. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Rajimehr, J. C. Young, and R. B. H. Tootell An anterior temporal face patch in human cortex, predicted by macaque maps PNAS, February 10, 2009; 106(6): 1995 - 2000. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Peng, M. E. Sereno, A. K. Silva, S. R. Lehky, and A. B. Sereno Shape Selectivity in Primate Frontal Eye Field J Neurophysiol, August 1, 2008; 100(2): 796 - 814. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Tanji and E. Hoshi Role of the Lateral Prefrontal Cortex in Executive Behavioral Control Physiol Rev, January 1, 2008; 88(1): 37 - 57. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Meyer, X.-L. Qi, and C. Constantinidis Persistent Discharges in the Prefrontal Cortex of Monkeys Naive to Working Memory Tasks Cereb Cortex, September 1, 2007; 17(suppl_1): i70 - i76. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. M. Romanski Representation and Integration of Auditory and Visual Stimuli in the Primate Ventral Lateral Prefrontal Cortex Cereb Cortex, September 1, 2007; 17(suppl_1): i61 - i69. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J Tate, H. Fischer, A. E Leigh, and K. M Kendrick Behavioural and neurophysiological evidence for face identity and face emotion processing in animals Phil Trans R Soc B, December 29, 2006; 361(1476): 2155 - 2172. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Sugihara, M. D. Diltz, B. B. Averbeck, and L. M. Romanski Integration of Auditory and Visual Communication Information in the Primate Ventrolateral Prefrontal Cortex J. Neurosci., October 25, 2006; 26(43): 11138 - 11147. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Inoue and A. Mikami Prefrontal Activity During Serial Probe Reproduction Task: Encoding, Mnemonic, and Retrieval Processes J Neurophysiol, February 1, 2006; 95(2): 1008 - 1041. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Tanibuchi and P. S. Goldman-Rakic Comparison of Oculomotor Neuronal Activity in Paralaminar and Mediodorsal Thalamus in the Rhesus Monkey J Neurophysiol, January 1, 2005; 93(1): 614 - 619. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. A. Greenberg and F. A. W. Wilson Functional Stability of Dorsolateral Prefrontal Neurons J Neurophysiol, August 1, 2004; 92(2): 1042 - 1055. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Hoshi and J. Tanji Area-Selective Neuronal Activity in the Dorsolateral Prefrontal Cortex for Information Retrieval and Action Planning J Neurophysiol, June 1, 2004; 91(6): 2707 - 2722. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. E. Hampson, T. P. Pons, T. R. Stanford, and S. A. Deadwyler Categorization in the monkey hippocampus: A possible mechanism for encoding information into memory PNAS, March 2, 2004; 101(9): 3184 - 3189. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R.N. Henson, Y. Goshen-Gottstein, T. Ganel, L.J. Otten, A. Quayle, and M.D. Rugg Electrophysiological and Haemodynamic Correlates of Face Perception, Recognition and Priming Cereb Cortex, July 1, 2003; 13(7): 793 - 805. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Tanibuchi and P. S. Goldman-Rakic Dissociation of Spatial-, Object-, and Sound-Coding Neurons in the Mediodorsal Nucleus of the Primate Thalamus J Neurophysiol, February 1, 2003; 89(2): 1067 - 1077. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Freedman, M. Riesenhuber, T. Poggio, and E. K. Miller Visual Categorization and the Primate Prefrontal Cortex: Neurophysiology and Behavior J Neurophysiol, August 1, 2002; 88(2): 929 - 941. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F.M. Mottaghy, M. Gangitano, R. Sparing, B.J. Krause, and A. Pascual-Leone Segregation of Areas Related to Visual Working Memory in the Prefrontal Cortex Revealed by rTMS Cereb Cortex, April 1, 2002; 12(4): 369 - 375. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Takeda and S. Funahashi Prefrontal Task-Related Activity Representing Visual Cue Location or Saccade Direction in Spatial Working Memory Tasks J Neurophysiol, January 1, 2002; 87(1): 567 - 588. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Z. Rapcsak, L. Nielsen, L. D. Littrell, E. L. Glisky, A. W. Kaszniak, and J. F. Laguna Face memory impairments in patients with frontal lobe damage Neurology, October 9, 2001; 57(7): 1168 - 1175. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Luciana, E. D. Burgund, M. Berman, and K. L. Hanson Effects of tryptophan loading on verbal, spatial and affective working memory functions in healthy adults J Psychopharmacol, July 1, 2001; 15(4): 219 - 230. [Abstract] [PDF]
|
|
|
|
|
|
M. Sakagami, K.-i. Tsutsui, J. Lauwereyns, M. Koizumi, S. Kobayashi, and O. Hikosaka A Code for Behavioral Inhibition on the Basis of Color, But Not Motion, in Ventrolateral Prefrontal Cortex of Macaque Monkey J. Neurosci., July 1, 2001; 21(13): 4801 - 4808. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Lebedev, D. K. Douglass, S. L. Moody, and S. P. Wise Prefrontal Cortex Neurons Reflecting Reports of a Visual Illusion J Neurophysiol, April 1, 2001; 85(4): 1395 - 1411. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Cornette, P. Dupont, G. Bormans, L. Mortelmans, and G.A. Orban Separate Neural Correlates for the Mnemonic Components of Successive Discrimination and Working Memory Tasks Cereb Cortex, January 1, 2001; 11(1): 59 - 72. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. H. Rammsayer Effects of Pharmacologically Induced Changes in NMDA-Receptor Activity on Long-Term Memory in Humans Learn. Mem., January 1, 2001; 8(1): 20 - 25. [Abstract] [Full Text]
|
|