Functional stability of dorsolateral prefrontal neurons.

Stable multiday recordings from the dorsolateral prefrontal cortex of 2 monkeys performing 2 Go/NoGo visual-discrimination tasks (one requiring well-learned responses, the other requiring learning) demonstrate that the majority of prefrontal neurons were "functionally stable". Recordings were made using a series of removable microdrives, each implanted for 3-6 mo, housing independently mobile electrodes. Action potential waveforms of 94 neurons were stable over 2-9 days; 66/94 (70%) of these cells responded each day, 22/94 (23%) never responded significantly, and 6/94 (6%) responded one day but not the next. Of 66 responsive neurons, 55 were selective for either Go or NoGo trials, individual stimuli, or eye movements. This selectivity was functionally stable (i.e., maintained) for 46/55 neurons across all recording days. Functional stability was also noted in terms of response strength (baseline firing rates compared with poststimulation firing rates) and event-related response timing. Two neurons with consistent responses in familiar testing conditions responded flexibly when the monkeys learned to make correct responses to novel stimuli. We conclude that the majority of prefrontal neurons were functionally stable during the performance of well-learned tasks. Such stability may be a general property of prefrontal neurons, given that neurons with 4 different types of task selectivity were found to be functionally stable. Conceptually similar studies based on long-term recordings in other cortical regions reached similar conclusions, suggesting that neurons throughout the brain are functionally stable.

[1]  R. H. Woodward,et al.  Cumulative Sum Techniques , 1964 .

[2]  J. Fuster Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[3]  E. M. Schmidt,et al.  Long-term chronic recording from cortical neurons , 1976, Experimental Neurology.

[4]  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 .

[5]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[6]  Lucien T. Thompson,et al.  Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats , 1990, Brain Research.

[7]  ET Rolls,et al.  Learning and memory is reflected in the responses of reinforcement- related neurons in the primate basal forebrain , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[9]  J. Fuster Frontal lobes , 1993, Current Opinion in Neurobiology.

[10]  H. Komatsu,et al.  Relationships between color, shape, and pattern selectivities of neurons in the inferior temporal cortex of the monkey. , 1993, Journal of neurophysiology.

[11]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[12]  P S Goldman-Rakic,et al.  Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

[14]  T. Robbins,et al.  Dissociable Forms of Inhibitory Control within Prefrontal Cortex with an Analog of the Wisconsin Card Sort Test: Restriction to Novel Situations and Independence from “On-Line” Processing , 1997, The Journal of Neuroscience.

[15]  M. Nicolelis,et al.  Reconstructing the Engram: Simultaneous, Multisite, Many Single Neuron Recordings , 1997, Neuron.

[16]  E. Miller,et al.  Neural Activity in the Primate Prefrontal Cortex during Associative Learning , 1998, Neuron.

[17]  R. F. Mayer The Prefrontal Cortex: Anatomy, Physiology and Neuropsychology of the Frontal Lobe, 3rd Edition. , 1999 .

[18]  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.

[19]  Justin C. Williams,et al.  Stability of chronic multichannel neural recordings: Implications for a long-term neural interface , 1999, Neurocomputing.

[20]  R. Spinks The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe, 3rd ed. , 2000 .

[21]  T. Bussey,et al.  Role of prefrontal cortex in a network for arbitrary visuomotor mapping , 2000, Experimental Brain Research.

[22]  Bao-Ming Li,et al.  Deficit in conditional visuomotor learning by local infusion of bicuculline into the ventral prefrontal cortex in monkeys , 2000, The European journal of neuroscience.

[23]  A Grinvald,et al.  Long-Term Optical Imaging and Spectroscopy Reveal Mechanisms Underlying the Intrinsic Signal and Stability of Cortical Maps in V1 of Behaving Monkeys , 2000, The Journal of Neuroscience.

[24]  Jerald D. Kralik,et al.  Techniques for long-term multisite neuronal ensemble recordings in behaving animals. , 2001, Methods.

[25]  F. A. Wilson,et al.  A microelectrode drive for long term recording of neurons in freely moving and chaired monkeys , 2003, Journal of Neuroscience Methods.

[26]  Hans Liljenström,et al.  Neural Stability and Flexibility: A Computational Approach , 2003, Neuropsychopharmacology.

[27]  M. Watanabe Prefrontal unit activity during associative learning in the monkey , 2004, Experimental Brain Research.