Abstract
The lateral habenula (LHb) is an epithalamic structure involved in signaling reward omission and aversive stimuli, and it inhibits dopaminergic neurons during motivated behavior. Less is known about LHb involvement in the acquisition and retrieval of avoidance learning. Our previous studies indicated that brief electrical stimulation of the LHb, time-locked to the avoidance of aversive footshock (presumably during the positive affective “relief” state that occurs when an aversive outcome is averted), inhibited the acquisition of avoidance learning. In the present study, we used the same paradigm to investigate different frequencies of LHb stimulation. The effect of 20 Hz vs. 50 Hz vs. 100 Hz stimulation was investigated during two phases, either during acquisition or retrieval in Mongolian gerbils. The results indicated that 50 Hz, but not 20 Hz, was sufficient to produce a long-term impairment in avoidance learning, and was somewhat more effective than 100 Hz in this regard. None of the stimulation parameters led to any effects on retrieval of avoidance learning, nor did they affect general motor activity. This suggests that, at frequencies in excess of the observed tonic firing rates of LHb neurons (>1–20 Hz), LHb stimulation may serve to interrupt the consolidation of new avoidance memories. However, these stimulation parameters are not capable of modifying avoidance memories that have already undergone extensive consolidation.
Highlights
Several neural systems implicated in reward-oriented approach are involved in the avoidance of negative outcomes (e.g. [1], [2]), and release of dopamine (DA) plays a role in both types of motivational processes [3], [4]
For both avoidance responding and latency, there was a significant main effect of session, F(4,164).77.2, p,.001, and a significant main effect of stimulation, F(3,41).6.94, p,.001. These effects were of little interest in light of the significant two-way interaction obtained for rate of successful avoidance responses, F(12,164) = 2.13, p = .02. This interaction term reflects a significant difference in the slopes of the learning curves across groups, with animals receiving 50 Hz or 100 Hz achieving lower levels of avoidance responding than animals receiving 20 Hz or no stimulation (Figure 2, top panel)
The results support a disruptive effect of lateral habenula (LHb) activation on negative reinforcement, with consequences for acquisition, but not retrieval, of an active avoidance response
Summary
Several neural systems implicated in reward-oriented approach are involved in the avoidance of negative outcomes (e.g. [1], [2]), and release of dopamine (DA) plays a role in both types of motivational processes [3], [4]. [1], [2]), and release of dopamine (DA) plays a role in both types of motivational processes [3], [4]. Among these systems, the lateral habenula (LHb) is functionally coupled to the dopaminergic systems during motivated behavior to signal negative affective states such as reward omission and punishment prediction [5]. The LHb is an epithalamic structure containing glutamatergic neurons involved in various processes such as the regulation of sleep, negative reward prediction, stress, learned helplessness, depression and behavioral inhibition [6], [7], [8], [5]. The LHb is anatomically positioned as a relay station between forebrain limbic-motor circuits and brainstem monoaminergic systems, and would appear to be a key node for rapidly influencing the selection of behavioral responses during learning [11], [12], [9], [13], [8]
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