Tagging items in spatial working memory: A unit-recording study in the rat medial prefrontal cortex

The rat medial prefrontal cortex has been suggested to be involved in executive functions and, more specifically, in working memory and response selection. Here, we looked for prefrontal neural correlates as rats performed a modified radial arm maze task that taxed such functions. Rats had to learn the position of four rewarded arms among eight, and visit each rewarded arm only once, thus avoiding repeated visits. In addition, rats were left on the maze after the four successful visits to baited arms until they had visited all the arms twice. Prefrontal neural activity was examined during choice periods, i.e. 2s before the rat entered the arms. We found that a substantial proportion of recorded medial prefrontal neurons were selectively activated before either the first or second visit to the arms irrespective of their reward status, thereby tagging already visited arms. These behavioral correlates show that, within the rodent medial prefrontal cortex, neuronal populations demonstrate behavioral correlates suggestive of its role in guiding prospective search behavior and thus executive functions.

[1]  P. Winn,et al.  Impaired delayed spatial win-shift behaviour on the eight arm radial maze following excitotoxic lesions of the medial prefrontal cortex in the rat , 2003, Behavioural Brain Research.

[2]  M. Jung,et al.  Dynamics of Population Code for Working Memory in the Prefrontal Cortex , 2003, Neuron.

[3]  Alan Baddeley,et al.  Frontal amnesia and the dysexecutive syndrome , 1988, Brain and Cognition.

[4]  B. McNaughton,et al.  Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. , 1998, Cerebral cortex.

[5]  Elizabeth E. Shillito,et al.  Exploratory Behaviour in the Short-Tailed Vole Microtus Agrestis , 1963 .

[6]  Bruno Poucet,et al.  Searching for spatial unit firing in the prelimbic area of the rat medial prefrontal cortex , 1997, Behavioural Brain Research.

[7]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  M. Wilson,et al.  Theta Rhythms Coordinate Hippocampal–Prefrontal Interactions in a Spatial Memory Task , 2005, PLoS biology.

[9]  Bruno Poucet,et al.  Involvement of the rat prefrontal cortex in cognitive functions: A central role for the prelimbic area , 2000, Psychobiology.

[10]  H. Eichenbaum,et al.  Medial Prefrontal Cortex Supports Recollection, But Not Familiarity, in the Rat , 2008, The Journal of Neuroscience.

[11]  R. Kesner Subregional analysis of mnemonic functions of the prefrontal cortex in the rat , 2000, Psychobiology.

[12]  M. Khamassi,et al.  Replay of rule-learning related neural patterns in the prefrontal cortex during sleep , 2009, Nature Neuroscience.

[13]  J. Webster,et al.  Frontal Lobe Lesions and Behavior* , 1981, Southern medical journal.

[14]  J. Seamans,et al.  Selective Roles for Hippocampal, Prefrontal Cortical, and Ventral Striatal Circuits in Radial-Arm Maze Tasks With or Without a Delay , 1997, The Journal of Neuroscience.

[15]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[16]  M. Buhot,et al.  Effects of medial septal or unilateral hippocampal inactivations on reference and working spatial memory in rats , 1994, Hippocampus.

[17]  Daniel Durstewitz,et al.  Comparing the prefrontal cortex of rats and primates: Insights from electrophysiology , 2008, Neurotoxicity Research.

[18]  A. Phillips,et al.  Ventral hippocampal involvement in temporal order, but not recognition, memory for spatial information , 2008, Hippocampus.

[19]  A. Phillips,et al.  Medial prefrontal cortex is involved in spatial temporal order memory but not spatial recognition memory in tests relying on spontaneous exploration in rats , 2004, Behavioural Brain Research.

[20]  E. Save,et al.  Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  H. Mallot,et al.  Reward modulates neuronal activity in the hippocampus of the rat , 2003, Behavioural Brain Research.

[22]  A. Kertesz Localization in neuropsychology , 1983 .

[23]  D. Olton,et al.  Animal Behavior Processes , 2022 .

[24]  G. Rebec,et al.  Subthalamic and striatal neurons concurrently process motor, limbic, and associative information in rats performing an operant task. , 2007, Journal of neurophysiology.

[25]  S. Mizumori,et al.  Neurons in rat medial prefrontal cortex show anticipatory rate changes to predictable differential rewards in a spatial memory task , 2001, Behavioural Brain Research.

[26]  J. Fuster The Prefrontal Cortex , 1997 .

[27]  J. Kubie A driveable bundle of microwires for collecting single-unit data from freely-moving rats , 1984, Physiology & Behavior.

[28]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[29]  Jeremy K. Seamans,et al.  Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. , 1995, Behavioral neuroscience.

[30]  Y. Sakurai,et al.  Multiple unit activity of prefrontal cortex and dorsomedial thalamus during delayed go/no-go alternation in the rat , 1986, Behavioural Brain Research.

[31]  A. S. Batuev,et al.  Unit activity of the medial wall of the frontal cortex during delayed performance in rats , 1990, Behavioural Brain Research.

[32]  Robert P. Vertes,et al.  Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat , 2006, Neuroscience.

[33]  Bruce L McNaughton,et al.  Selective delay activity in the medial prefrontal cortex of the rat: contribution of sensorimotor information and contingency. , 2007, Journal of neurophysiology.

[34]  Colin Gemmell,et al.  Deep layer prefrontal cortex unit discharge in a cue-controlled open-field environment in the freely-moving rat , 2002, Behavioural Brain Research.