Prelimbic and Infralimbic Neurons Signal Distinct Aspects of Appetitive Instrumental Behavior

Burgos-Robles, Anthony; Bravo-Rivera, Héctor; Quirk, Gregory J.

doi:10.1371/journal.pone.0057575

Cited by 82 publications

(74 citation statements)

References 30 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…PL responses were equally divided between excitation and inhibition, whereas most IL responses were inhibitory. PL and IL neurons also fired differentially around the reward: PL neurons were excited at well entry and inhibited during consumption, whereas IL neurons were inhibited at well entry and excited during consumption, in line with a recent report (15). The time course of extinction-related changes in RS signaling also differed across PL and IL neurons: IL neurons shifted to signaling withholding more rapidly than PL neurons (Fig.…”

Section: Discussionsupporting

confidence: 89%

Prefrontal neurons encode context-based response execution and inhibition in reward seeking and extinction

Moorman

Aston‐Jones

2015

Proc. Natl. Acad. Sci. U.S.A.

125

View full text Add to dashboard Cite

The prefrontal cortex (PFC) guides execution and inhibition of behavior based on contextual demands. In rodents, the dorsal/ prelimbic (PL) medial PFC (mPFC) is frequently considered essential for execution of goal-directed behavior ("go") whereas ventral/ infralimbic (IL) mPFC is thought to control behavioral suppression ("stop"). This dichotomy is commonly seen for fear-related behaviors, and for some behaviors related to cocaine seeking. Overall, however, data for reward-directed behaviors are ambiguous, and few recordings of PL/IL activity have been performed to demonstrate single-neuron correlates. We recorded neuronal activity in PL and IL during discriminative stimulus driven sucrose seeking followed by multiple days of extinction of the reward-predicting stimulus. Contrary to a generalized PL-go/IL-stop hypothesis, we found cue-evoked activity in PL and IL during reward seeking and extinction. Upon analyzing this activity based on resultant behavior (lever press or withhold), we found that neurons in both areas encoded contextually appropriate behavioral initiation (during reward seeking) and withholding (during extinction), where context was dictated by response-outcome contingencies. Our results demonstrate that PL and IL signal contextual information for regulation of behavior, irrespective of whether that involves initiation or suppression of behavioral responses, rather than topographically encoding go vs. stop behaviors. The use of context to optimize behavior likely plays an important role in maximizing utility-promoting exertion of activity when behaviors are rewarded and conservation of energy when not.he prefrontal cortex (PFC) is involved in directing behavior and inhibiting inappropriate responses (1-4). Rodent medial PFC (mPFC) is functionally heterogeneous: prelimbic cortex (PL) is thought to be involved in behavioral execution, and infralimbic cortex (IL) in behavioral suppression, particularly during extinction (4). Fear conditioning studies support this dichotomy. PL stimulation elicits, and inactivation impairs, conditioned fear expression, and PL neurons fire during fear-related cues. Conversely, IL stimulation enhances, and inactivation blocks, extinction of fear conditioning, and IL neurons fire for extinguished cues that previously predicted an aversive stimulus (5, 6).A similar dichotomy is proposed for appetitive behaviors, although support for this is not unequivocal (7). PL inactivation during discriminative stimulus (DS)-driven reward-seeking reduces cue-driven behaviors (8). However, PL inactivation also increases nonspecific (8) and premature lever responding (9, 10), and PL is important in inhibiting responses during a stop-signal reaction time task (11). IL inactivation during DS task performance increases responses generally, including those triggered by a nonrewarded stimulus (NS) (8), increases premature responding on five-choice serial reaction time tasks (12), and increases spontaneous recovery and reinstatement (13). Cocaine seeking is also associated with activation ...

show abstract

Section: Discussionsupporting

confidence: 89%

Prefrontal neurons encode context-based response execution and inhibition in reward seeking and extinction

Moorman

Aston‐Jones

2015

Proc. Natl. Acad. Sci. U.S.A.

125

View full text Add to dashboard Cite

show abstract

“…Therefore these structures that are important for regulating behavior in appetitive-related tasks are also important earlier when the initial cue-food associations are formed. More generally, our findings add to accumulating evidence implicating these regions in the control of feeding and appetitive-related behaviors (Corbit and Balleine, 2003; Petrovich et al, 2005;Nair et al, 2011; Mena et al, 2011, 2013; Cifani et al, 2012; Burgos-Robles et al, 2013; Calu et al, 2013; Land et al, 2014). …”

Section: Discussionsupporting

confidence: 77%

Appetitive associative learning recruits a distinct network with cortical, striatal, and hypothalamic regions

2015

View full text Add to dashboard Cite

The amygdala, prefrontal cortex, striatum and other connected forebrain areas are important for reward-associated learning and subsequent behaviors. How these structurally and functionally dissociable regions are recruited during initial learning, however, is unclear. Recently, we showed amygdalar nuclei were differentially recruited across different stages of cue-food associations in a Pavlovian conditioning paradigm. Here, we systematically examined Fos induction in the forebrain, including areas associated with the amygdala, during early (day 1) and late (day 10) training sessions of cue-food conditioning. During training, rats in the conditioned group received tone-food pairings, while controls received presentations of the tone alone in the conditioning chamber followed by food delivery in their home cage. We found that a small subset of telencephalic and hypothalamic regions were differentially recruited during the early and late stages of training, suggesting evidence of learning induced plasticity. Initial tone-food pairings recruited solely the amygdala, while late tone-food pairings came to induce Fos in distinct areas within the medial and lateral prefrontal cortex, the dorsal striatum, and the hypothalamus (lateral hypothalamus and paraventricular nucleus). Furthermore, within the perifornical lateral hypothalamus, tone-food pairings selectively recruited neurons that produce the orexigenic neuropeptide orexin/hypocretin. These data show a functional map of the forebrain areas recruited by appetitive associative learning and dependent on experience. These selectively activated regions include interconnected prefrontal, striatal, and hypothalamic regions that form a discrete but distributed network that is well placed to simultaneously inform cortical (cognitive) processing and behavioral (motivational) control during cue-food learning.

show abstract

“…Waveforms were recorded during pretone, tone, and posttone periods, each lasting 30 s. Single units were isolated using principal component analysis and template matching (Offline Sorter; Plexon). Both automated and manual correction processing techniques were applied to sort spikes (see Burgos-Robles et al, 2013;Sotres-Bayon et al, 2012). Automated processing was carried out using a valleyseeking scan algorithm (Offline Sorter; Plexon), one channel at a time, and then evaluated using sort quality metrics.…”

Section: Single-unit Recordingsmentioning

confidence: 99%

Hippocampal–Prefrontal BDNF and Memory for Fear Extinction

Rosas-Vidal

Monte

Sotres-Bayón

et al. 2014

Neuropsychopharmacol

166

168

View full text Add to dashboard Cite

Infusing brain-derived neurotrophic factor (BDNF) into the infralimbic (IL) prefrontal cortex is capable of inducing extinction. Little is known, however, about the circuits mediating BDNF effects on extinction or the extent to which extinction requires BDNF in IL. Using local pharmacological infusion of BDNF protein, or an antibody against BDNF, we found that BDNF in the IL, but not prelimbic (PL) prefrontal cortex, is both necessary and sufficient for fear extinction. Furthermore, we report that BDNF in IL can induce extinction of older fear memories (14 days) as well as recent fear memories (1 day). Using immunocytochemistry, we show that BDNF is increased in the ventral hippocampus (vHPC), but not IL or PL, following extinction training. Finally, we observed that infusing BDNF into the vHPC increased the firing rate of IL, but not PL neurons in fear conditioned rats. These findings indicate that an extinction-induced increase in BDNF within the vHPC enhances excitability in IL targets, thereby supporting extinction memories.

show abstract

Prelimbic and Infralimbic Neurons Signal Distinct Aspects of Appetitive Instrumental Behavior

Cited by 82 publications

References 30 publications

Prefrontal neurons encode context-based response execution and inhibition in reward seeking and extinction

Prefrontal neurons encode context-based response execution and inhibition in reward seeking and extinction

Appetitive associative learning recruits a distinct network with cortical, striatal, and hypothalamic regions

Hippocampal–Prefrontal BDNF and Memory for Fear Extinction

Contact Info

Product

Resources

About