Differential Contribution of Hippocampal Circuits to Appetitive and Consummatory Behaviors during Operant Conditioning of Behaving Mice

Abstract

Operant conditioning is a type of associative learning involving different and complex sensorimotor and cognitive processes. Because the hippocampus has been related to some motor and cognitive functions involved in this type of learning (such as object recognition, spatial orientation, and associative learning tasks), we decided to study in behaving mice the putative changes in strength taking place at the hippocampal CA3-CA1 synapses during the acquisition and performance of an operant conditioning task. Mice were chronically implanted with stimulating electrodes in the Schaffer collaterals and with recording electrodes in the hippocampal CA1 area and trained to an operant task using a fixed-ratio (1:1) schedule. We recorded the field EPSPs (fEPSPs) evoked at the CA3-CA1 synapse during the performance of appetitive (going to the lever, lever press) and consummatory (going to the feeder, eating) behaviors. In addition, we recorded the local field potential activity of the CA1 area during similar behavioral displays. fEPSPs evoked at the CA3-CA1 synapse presented larger amplitudes for appetitive than for consummatory behaviors. This differential change in synaptic strength took place in relation to the learning process, depending mainly on the moment in which mice reached the selected criterion. Thus, selective changes in CA3-CA1 synaptic strength were dependent on both the behavior display and the learning stage. In addition, significant changes in theta band power peaks and their corresponding discrete frequencies were noticed during these behaviors across the sequence of events characterizing this type of associative learning but not during the acquisition process.

Functional basis of associative learning and its relationships with long-term potentiation evoked in the involved neural circuits: Lessons from studies in behaving mammals

“…In contrast, it has been recently shown that the hippocampus is not very much involved in the entire process of the acquisition of instrumental learning tasks (Jurado-Parras, Jurado-Parras et al, 2013), although the CA3-CA1 is modulated in strength by the performance of specific appetitive (e.g., pressing a lever in order to obtain a piece of food) vs. consummatory (e.g., eating the collected pellet) behaviors . This involvement of the hippocampus in specific behaviors related to operant conditioning tasks is extensible to appetitive reinforcements (pressing a lever to obtain an electrical stimulation of a positive reinforcing center, such as the medial septum) vs. internal ones (in order to receive the self-stimulation) (Vega-Flores, Rubio, Jurado-Parras, Gómez-Climent, Hampe, Manto, Soriano, Pascual, Gruart, & Delgado-García, 2014).…”

“…Particular attention will be paid to the contribution of specific hippocampal, prefrontal, and other cortical and subcortical circuits to the acquisition to the two main types of associative learning, represented by the classical conditioning of eyelid responses, and selective operant conditioning tasks (CarreteroGuillén et al, in press;Eleore, López-Ramos, Yi, & DelgadoGarcía, 2007;Gruart et al, in press;Jurado-Parras, Sánchez-Campusano, Castellanos, del-Pozo, Gruart, Delgado-García, 2013;Leal-Campanario, Delgado-García, & Gruart, 2013).…”

The outward spiral: a vicious cycle model of obesity and cognitive dysfunction

“…For example, the hippocampus has been implicated in resolving approach-avoidance discrepancies in situations in which two opposing response tendencies are experienced simultaneously [15, 16]. Other findings suggest adaptive response selection is based on the contribution of the hippocampus to the context-dependent inhibition of approach tendencies [14, 17, 18]. The retrieval of situationally-appropriate memories by contextual cues and the reduction of interference by memories formed in other contexts are also considered functions of the hippocampus [19, 20].…”

Functional states of rat cortical circuits during the unpredictable availability of a reward-related cue

“…Changes in synaptic weights during the acquisition of classical24 and instrumental34 conditioning paradigms have been reported for the above-mentioned neural centers, as well as during the performance of inhibitory avoidance learning39 and object recognition4041 tasks. In addition, brain state can change rapidly such as in the case of attention, and transiently modulate neural responsiveness4243444546.…”

“…Within the hippocampus, the CA1 region has been related to appetitive and consummatory behaviors during operant conditioning tasks34, as well as during novelty detection3536. The SUB is a hippocampal output structure receiving synaptic excitation from CA1 pyramidal cells, and represents an important connecting node for processing spatial information and body movements.…”