The anterior cingulate cortex (ACC) has been implicated in both preparatory attention (i.e., selecting behaviorally relevant stimuli) and in detecting errors. We recorded from the rat ACC and medial prefrontal cortex (mPFC), which is functionally homologous to the primate dorsolateral PFC, during an attention task. The three-choice serial reaction time task requires a rat to orient toward and divide attention between three brief (300 ms duration) light stimuli presented in random order across nose poke holes in an operant chamber. In both the ACC and mPFC, we found that neural activity was related to the level of preparatory (precue) attention and subsequent correct or incorrect choice, in that the magnitude of the single units' response to the cue was lower on incorrect trials and was not different than baseline on unattended trials. This preparatory neural activity consisted of both excitatory and inhibitory phasic responses. The number of units responding to the cue was similarly graded, in that fewer units exhibited phasic responses to the cue on incorrect and unattended trials, compared with correct trials. Although preparatory activity was found in both the ACC and mPFC, activity after incorrect nose pokes, which may be related to error detection, were only observed in the ACC. Thus, during the same behavioral sequence, the ACC encodes both error-related events and preparatory attention, whereas the mPFC only participates in preparatory attention. The finding of substantial inhibitory activity during the preparatory period suggests a critical role for inhibition of pyramidal cells in PFC-mediated cognitive functions.

Dopamine influences affective, motor and cognitive processing, and multiple forms of learning and memory. This multifaceted functionality, which operates across long temporal windows, is broader than the narrow and temporally constrained role often ascribed to dopamine neurons as reward prediction error detectors. Given the modulatory nature of dopamine neurotransmission, that dopamine release is activated by both aversive and appetitive stimuli, and that dopamine receptors are often localized extrasynaptically, a role for dopamine in transmitting precise error signals has been questioned. Here we recorded from ventral tegmental area (VTA) neurons, while exposing rats to novel stimuli that were predictive of an appetitive or aversive outcome in the same behavioral session. The VTA contains dopamine and γ-aminobutyric acid (GABA) neurons that project to striatal and cortical regions and are strongly implicated in learning and affective processing. The response of VTA neurons, regardless of whether they had putative dopamine or GABA waveforms, transformed flexibly as animals learned to associate novel stimuli from different sensory modalities to appetitive or aversive outcomes. Learning the appetitive association led to larger excitatory VTA responses, whereas acquiring the aversive association led to a biphasic response of brief excitation followed by sustained inhibition. These responses shifted rapidly as outcome contingencies changed. These data suggest that VTA neurons interface sensory information with representational memory of aversive and appetitive events. This pattern of plasticity was not selective for putative dopamine neurons and generalized to other cells, suggesting that the temporally precise information transfer from the VTA may be mediated by faster acting GABA neurons. Keywords addiction; freely moving rat; memory; reward; schizophrenia © 2010 Federation of European Neuroscience Societies and Blackwell Publishing LtdCorrespondence: Bita Moghaddam, as above. bita@pitt.edu. Supporting Information Additional supporting information may be found in the online version of this article: Fig. S1. Example of VTA recording data and recording site. Fig. S2. The difference in responses to CSav and CS−. Fig. S3. Changes in the proportion of responsive neurons to either CS during sessions 1-16. Fig. S4. Examples of neurons recorded on the same channel during several sessions across the contingency reversal. Fig. S5. Effects of sugar pellet delivery and shock on VTA neurons. Fig. S6. VTA neural response profiles to CSs and USs. Fig. S7. Comparison of the neural responses of different firing rate VTA neuron groups. Please note: As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset by Wiley-Blackwell.

We have shown previously that stimulus-induced modulation of noise correlation in rat somatosensory cortex conveys additional information about the delivery of tactile stimulation. Here we investigated whether noise correlation is also modulated by an external sensory stimulus in rat prefrontal cortex and, if so, whether such modulation conveys additional information on stimulus delivery. Noise correlation was significantly reduced after the onset of a conditional stimulus (auditory tone) that signaled an electric foot shock in the prefrontal cortex. However, noise correlation contributed little to the transmission of information on stimulus delivery. These results indicate that a meaningful sensory stimulus reduces noise correlation in rat prefrontal cortex, but such modulation does not play a significant role in conveying information on stimulus delivery.