Orbitofrontal Ensemble Activity Monitors Licking and Distinguishes Among Natural Rewards

Abstract

The classification of rhythmic licking into clusters has proved to be useful for characterizing brain mechanisms that modulate the ingestion of natural rewards (sucrose and water). One cortical area that is responsive to rewarding stimuli is the orbitofrontal cortex (OFC). However, it is not presently known how OFC neurons respond while rodents freely lick for natural rewards and whether these responses are related to the structure of licking clusters. We addressed these issues by showing that temporary inactivation of the OFC decreases the duration and increases the number of clusters and that the activity of OFC neurons changed at precise times before, during, and after the cluster terminates. Furthermore, analysis of the activity of OFC neuronal ensembles showed that they could discriminate cluster onset from termination, predict when a behaving animal will begin a cluster, and distinguish and anticipate between natural rewards. These results provide a new role for the OFC in influencing licking clusters and anticipating specific rewards.

Theta-Band Phase Locking of Orbitofrontal Neurons during Reward Expectancy

“…In rats, expectancy can be tightly coupled to direct motor consequences such as anticipatory licking (Neafsey et al, 1986;Gutierrez et al, 2006Gutierrez et al, , 2010. We found no systematic relationship between individual lick responses and theta activity in LFP traces (i.e., individual licks were not systematically associated with theta oscillations).…”

“…Previously, neural activity in amygdala and mPFC was shown to synchronize in the theta band (Pape et al, 1998;Siapas et al, 2005;Paz et al, 2008). We hypothesize that the synaptic updating process in OFC and related circuits underlying modification of stored associations may rely on spike-timing-dependent plasticity (STDP) (Levy and Steward, 1983;Cassenaer and Laurent, 2007) during coherent theta-band activity, which could be boosted by repetitive licking (Gutierrez et al, 2006). Under this hypothesis, the firing patterns phase locked to OFC theta oscillations convey a synchronized reward expectancy signal to target areas, which may or may not be continued into the period of the actual outcome, with significant consequences for learning.…”

“…In addition to correlating with reward expectancy, the question arises whether theta-band phase locking is also related to licking behavior (Gutierrez et al, 2006(Gutierrez et al, , 2010. Unlike licking, which occurred across both waiting and delivery periods, thetaband phase locking was selectively enhanced only during the sucrose anticipation period (Fig.…”

“…We found no systematic relationship between individual lick responses and theta activity in LFP traces (i.e., individual licks were not systematically associated with theta oscillations). However, based on the observation by Gutierrez et al (2006) that OFC spiking activity may correlate with clusters of lick responses, we checked whether the frequency of licking was associated with theta-band phase locking under the respective trial conditions (supplemental Fig. S4, available at www.jneurosci.org as supplemental material).…”

Neuronal Activity in the Primary Somatosensory Thalamocortical Loop Is Modulated by Reward Contingency during Tactile Discrimination

“…3,5,10), which was measured in the time window from Ϫ3 to Ϫ2 s before the nose-poke photobeam. Magnitudes of the responses during the presentation of the stimulus were defined as the increase (excited cells) or decrease (inhibited cells) in firing rates (in hertz) relative to the baseline firing levels using a program developed by Mike Wiest and Ranier Gutierrez (Wiest et al, 2005;Gutierrez et al, 2006). The duration, also calculated for inhibited and excited cells, was defined as the time during which significant firing changes occurred ( p Ͻ 0.01).…”