Neural correlates of auditory recognition memory in primate lateral prefrontal cortex

Neuroscience

Volumn 244, Issue , 2013, Pages 62-76

  Plakke, B ^a   Ng, C W ^a   Poremba, A ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Area 46; Delay; Matching to sample; Rhesus macaque; Vocalizations; Working memory

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; AUDITORY DISCRIMINATION; AUDITORY MEMORY; AUDITORY STIMULATION; BRAIN NERVE CELL; EVOKED AUDITORY RESPONSE; FEMALE; LATERAL PREFRONTAL CORTEX; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; REWARD; RHESUS MONKEY; SINGLE UNIT ACTIVITY; STIMULUS RESPONSE; VISUAL MEMORY; WORKING MEMORY;

ACOUSTIC STIMULATION; ANIMALS; DECISION MAKING; EVOKED POTENTIALS, AUDITORY; FEMALE; MACACA MULATTA; MALE; MEMORY, SHORT-TERM; NEURONS; PREFRONTAL CORTEX; RECOGNITION (PSYCHOLOGY); REWARD;

EID: 84877330864     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.04.002     Document Type: Article

References (89)

1. Arnott S.R., Binns M.A., Grady C.L., Alain C. Assessing the auditory dual-pathway in humans. Neuroimage 2004, 1:401-408.
2. Arnott S.R., Grady C.L., Hevenor S.J., Graham S., Alain C. The functionally organization of auditory working memory as revealed by fMRI. J Cogn Neurosci 2005, 17:819-831.
3. Asaad W.F., Rainer G., Miller E.K. Neural activity in the primate prefrontal cortex during associative learning. Neuron 1998, 21:1399-1407.
4. Asaad W.F., Rainer G., Miller E.K. Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol 2000, 84:451-459.
5. Azuma M., Suzuki H. Properties and distribution of auditory neurons in the dorsolateral prefrontal cortex of the alert monkey. Brain Res 1984, 298:343-346.
6. Barcelo F., Knight R.T. An information-theoretical approach to contextual processing in the human brain: evidence from prefrontal lesions. Cereb Cortex 2007, 17:i51-i60.
7. Bodner M., Kroger J., Fuster J.M. Auditory memory cells in dorsolateral prefrontal cortex. NeuroReport 1996, 7:1905-1908.
8. Buffalo E.A., Ramus S.J., Squire L.R., Zola S.M. Perception and recognition memory in monkeys following lesions of area TE and perirhinal cortex. Learn Mem 2000, 7:1905-1908.
9. Cohen J.D., Peristein W.M., Braver T.S., Nystrom L.E., Noll D.C., Jonides J., Smith E.E. Temporal dynamics of brain activation during a working memory task. Nat Neurosci 1997, 386:604-608.
10. Colombo M., Graziano M. Effects of auditory and visual interference on auditory-visual delayed matching to sample in monkeys (Macaca fasicularis). Behav Neurosci 1994, 108(3):636-639.
11. Constantindis C., Franowicz M.N., Goldman-Rakic P.S. The sensory nature of mnemonic representation in the primate prefrontal cortex. Nat Neurosci 2001, 4:311-316.
12. Courtney S.M., Ungerleider L.G., Keil K., Haxby J.V. Object and spatial visual working memory activate separate neural systems in human cortex. Cereb Cortex 1996, 6:39-49.
13. Davachi L., Goldman-Rakic P.S. Primate rhinal cortex participates in both visual recognition and working memory tasks: functional mapping with 2-DG. J Neurophysiol 2001, 85(6):2590-2601.
14. D'Esposito M., Postle B.R., Rympa B. Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp Br Res 2000, 133:3-11.
15. D'Esposito M., Cooney J.W., Gazzaley A., Gibbs S.E.B., Postle B.R. Is the prefrontal cortex necessary for delay task performance? Evidence from lesion and fMRI data. J Int Neuropsych Soc 2006, 12:248-260.
16. Freedman D.J., Riesenhuber M., Poggio T., Miller E.K. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 2001, 291:312-316.
17. Freedman D.J., Riesenhuber M., Poggio T., Miller E.K. Visual categorization and the primate prefrontal cortex: neurophysiology and behavior. J Neurophysiol 2002, 88:929-941.
18. Freedman D.J., Riesenhuber M., Poggio T., Miller E.K. A comparison of primate prefrontal and inferior temporal cortices during visual categorization. J Neurosci 2003, 23(12):5235-5246.
19. Fritz J., Mishkin M., Saunders R.C. In search of an auditory engram. Proc Natl Acad Sci USA 2005, 102:9359-9364.
20. Funahashi S., Bruce C.J., Goldman-Rakic P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 1989, 61:331-349.
21. Funahashi S., Bruce C.J., Goldman-Rakic P.S. Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 1991, 65:1464-1483.
22. Fuster J.M. Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol 1973, 36:61-78.
23. Fuster J.M. The prefrontal cortex 2008, Academic Press, Boston. 4th ed.
24. Fuster J.M., Bauer R.H., Jervey J.P. Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks. Exp Neurol 1982, 77:679-694.
25. Fuster J.M., Bodner M., Kroger J.K. Cross-modal and cross-temporal associations in neurons of frontal cortex. Nat Neurosci 2000, 405:347-351.
26. Gazzaley A., Rissman J., Cooney J., Rutman A., Seibert T., Clapp W., D'Esposito M. Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. Cereb Cortex Suppl 2007, 1:i25-i35.
27. Gifford G.W., MacLean K.A., Hauser M.D., Cohen Y.E. The neurophysiology of functionally meaningful categories: macaque ventrolateral prefrontal cortex plays a critical role in spontaneous categorization of species-specific vocalizations. J Cogn Neurosci 2005, 17:1471-1482.
28. Goldman P.S., Rosvold H.E. Localization of function within the dorsolateral prefrontal cortex of the Rhesus monkey. Exp Neurol 1970, 27:291-304.
29. Goldman-Rakic P.S. Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. Handbook of physiology 1987, Amer Physiol Soc, Bethesda (MD).
30. Hasegawa R., Sawaguchi T., Kubota K. Monkey prefrontal neuronal activity coding the forthcoming saccade in an oculomotor delayed matching-to-sample task. J Neurophysiol 1998, 79:322-333.
31. Heffner H.E., Heffner R.S. Temporal lobe lesions and perception of species-specificvocalizations by macaques. Science 1984, 226(4670):75-76.
32. Heffner He, Heffner R.S. Hearing loss in Japanese macaques following bilateral auditory cortex lesions. J Neurophysiol 1986, 55(2):256-271.
33. Hikosaka K., Watanabe M. Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. Cereb Cortex 2000, 10:263-271.
34. Iba M., Sawaguchi T. Neuronal activity representing visuospatial mnemonic processes associated with target selection in the monkey dorsolateral prefrontal cortex. Neurosci Res 2002, 43:9-22.
35. Kaas J.H., Hackett T.A. Subdivisions of auditory cortex and levels of processing in primates. Audiol Neuro-otol 1998, 3:73-85.
36. Kennerley S.W., Wallis J.D. Reward-dependent modulation of working memory in lateral prefrontal cortex. J Neurosci 2009, 29:3259-3270.
37. Kennerley S.W., Dahmubed A.F., Sara A.H., Wallis J.D. Neurons in the frontal lobe encode the value of multiple decision variables. J Cogn Neurosci 2009, 21:1162-1178.
38. Kikuchi-Yorioka Y., Sawaguchi T. Parallel visuospatial and audiospatial working memory processes in the monkey dorsolateral prefrontal cortex. Nat Neurosci 2000, 3:1075-1076.
39. Kojima S., Goldman-Rakic P.S. Delay-related activity of prefrontal neurons in Rhesus monkeys performing delayed response. Brain Res 1982, 248:43-49.
40. Kowalska D.M., Dusmierek P., Kosmal A., Mishkin M. Neither perirhinal/entorhinal nor hippocampal lesions impair short-term auditory recognition memory in dogs. Neuroscience 2001, 104(4):965-978.
41. Leon M.I., Shadlen M.N. Effect of expected reward magnitude on the response of neurons in the dorsolateral prefrontal cortex of the macaque. Neuron 1999, 24:15-425.
42. Málková L., Bachevalier J., Mishkin M., Saunders R.C. Neurotoxic lesions of perirhinal cortex impair visual recognition memory in rhesus monkeys. NeuroReport 2001, 12(9):1913-1917.
43. Meunier M., Bachevalier J., Mishkin M., Murray E.A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 1993, 13(12):5418-5432.
44. Meunier M., Hadfield W., Bachevalier J., Murray E.A. Effects of rhinal cortex lesions combined with hippocampectomy on visual recognition memory in rhesus monkeys. J Neurophysiol 1996, 75(3):1190-1205.
45. Miller E.K. The prefrontal cortex and cognitive control. Nat Rev Neurosci 2000, 1:59-65.
46. Miller E.K., Erickson C.A., Desimone R. Neural mechanisms of visual working memory in prefrontal cortex of the Macaque. J Neurosci 1996, 16:5154-5167.
47. Mishkin M., Delacour J. An analysis of short-term visual memory in the monkey. J Exp Psychol Anim Behav Process 1975, 1(4):326-334.
48. Mishkin M., Ungerleider L.G., Macko K.A. Object vision and spatial vision: two cortical pathways. Trends Neurosci 1983, 6:414-417.
49. Muñoz M., Mishkin M., Saunders R.C. Resection of the medial temporal lobe disconnects the rostral superior temporal gyrus from some of its projection targets in the frontal lobe and thalamus. Cereb Cortex 2009, 19:2114-2130.
50. Murray E.A., Mishkin M. Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy. J Neurosci 1986, 6(7):1991-2003.
51. Murray E.A., Mishkin M. Severe tactual memory deficits in monkeys after combined removal of the amygdala and hippocampus. Brain Res 1983, 270(2):340-344.
52. Newman J.D., Lindsley D.F. Single unit analysis of auditory processing in squirrel monkey frontal cortex. Exp Br Res 1976, 25:169-181.
53. Ng C.W., Plakke B., Poremba A. Primate auditory recognition memory performance varies with sound type. Hearing Res 2009, 256:64-74.
54. Nieder A., Freedman D.J., Miller E.K. Representation of the quantity of visual items in the primate prefrontal cortex. Science 2002, 297(5587):1708-1711.
55. Otto T., Eichenbaum H. Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. Behav Neurosci 1992, 106(5):762-775.
56. Owen A.M., Downes J.J., Sahakian B.J., Polkey C.E., Robbins T.W. Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia 1990, 28:1021-1034.
57. Owen A.M., Sahakian B.J., Semple J., Polkey C.E., Robbins T.W. Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia 1995, 33:1-24.
58. Pasupathy A., Miller E.K. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nat Neurosci 2005, 433:873-876.
59. Petersen M.R., Beecher M.D., Zoloth S.R., Green S., Marler P.R., Moody D.B., Stebbins W.C. Neural lateralization of vocalizations by Japanese macaques: communicative significance is more important than acoustic structure. Behav Neurosci 1984, 98(5):779-790.
60. Poremba A., Mishkin M. Exploring the extent and function of higher-order auditory cortex in rhesus monkeys. Hearing Res 2007, 229:14-23.
61. Poremba A., Saunders R.C., Crane A.M., Cook M., Sokoloff L., Mishkin M. Functional mapping of the primate auditory system. Science 2003, 299:568-572.
62. Poremba A., Malloy M., Saunders R.C., Carson R.E., Herscovitch P., Mishkin M. Species-specific calls evoke asymmetric activity in the monkey's temporal poles. Nat Neurosci 2004, 427(6973):448-451.
63. Quintana J., Fuster J.M. From perception to action: temporal integrative functions of prefrontal and parital neurons. Cereb Cortex 1999, 9:213-221.
64. Rainer G., Asaad W.F., Miller E.K. Selective representation of relevant information by neurons in the primate prefrontal cortex. Nat Neurosci 1998, 393:577-579.
65. Rainer G., Rao S.C., Miller E.K. Prospective coding for objects in primate prefrontal cortex. J Neurosci 1999, 19:5493-5505.
66. Rämä P., Courtney S.M. Functional topography of working memory for face or voice identity. NeuroImage 2005, 24:224-234.
67. Rämä P., Poremba A., Sala J.B., Yee L., Malloy M., Mishkin M., Courtney S.M. Dissociable functional cortical topographies for working memory maintenance of voice identity and location. Cereb Cortex 2004, 14:768-780.
68. Ranganath C., Cohen M.X., Dam C., D'Esposito M. Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. J Neurosci 2004, 24:3917-3925.
69. Rao S.C., Rainer G., Miller E.K. Integration of what and where in the primate prefrontal cortex. Science 1997, 276:821-824.
70. Rauschecker J.P., Tian B. Mechanisms and streams for processing of "what" and "where" in auditory cortex. Proc Natl Acad Sci 2000, 97:11800-11806.
71. Romanski L.M., Goldman-Rakic P.S. An auditory domain in primate prefrontal cortex. Nat Neurosci 2002, 5:15-16.
72. Romanski L.M., Giguere M., Bates J.F., Goldman-Rakic P.S. Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. J Comp Neurol 1997, 379:313-332.
73. Romanski L.M., Tian B., Fritz J., Mishkin M., Goldman-Rakic P.S., Rauschecker J.P. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 1999, 2:1131-1136.
74. Romanski L.M., Averbeck B.B., Diltz M. Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. J Neurophysiol 2005, 93:734-747.
75. Russ B.E., Orr L.E., Cohen Y.E. Prefrontal neurons predict choices during an auditory same-different task. Curr Biol 2008, 18:1483-1488.
76. Schulze K, Vargha-Khadem F, Mishkin M. (2012) Test of a motor theory of long-term auditory memory. Proc Natl Acad Sci 109(18):7121-7125.
77. Scott B.H., Mishkin M., Yin P. Monkeys have a limited form of short-term memory in audition. PNAS 2012, 109(30):12237-12241.
78. Squire L.R., Schmolck H., Stark S.M. Impaired auditory recognition memory in amnesic patients with medial temporal lobe lesions. Learn Mem 2001, 8(5):252-256.
79. Suzuki W.A., Zola-Morgan S., Squire L.R., Amaral D.G. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J Neurosci 1993, 13(6):2430-2451.
80. Suzuki W.A., Miller E.K., Desimone R. Object and place memory in the macaque entorhinal cortex. J Neurophysiol 1997, 78(2):1062-1081.
81. Wallis J.D., Miller E.K. Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 2003, 18:2069-2081.
82. Wallis J.D., Anderson K.C., Miller E.K. Single neurons in prefrontal cortex encode abstract rules. Nat Neurosci 2001, 411:953-956.
83. Warden M.R., Miller E.K. The representation of multiple objects in prefrontal neuronal delay activity. Cereb Cortex 2007, 17:i41-i50.
84. Warden M.R., Miller E.K. Task-dependent changes in short-term memory in the prefrontal cortex. J Neurosci 2010, 30:15801-15810.
85. Watanabe M. Frontal units of the monkey coding the associative significance of visual and auditory stimuli. Exp Br Res 1992, 89:233-247.
86. Watanabe M. Reward expectancy in primate prefrontal neurons. Nat Neurosci 1996, 382:629-632.
87. White I.M., Wise S.P. Rule-dependent neuronal activity in the prefrontal cortex. Exp Br Res 1999, 126:315-335.
88. Yassa M.A., Stark C.E. Multiple signals of recognition memory in the medial temporal lobe. Hippocampus 2008, 18(9):945-954.
89. Zola-Morgan S., Squire L.R., Amaral D.G. Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys. J Neurosci 1989, 9(3):898-913.