Amygdala input differentially influences prefrontal local field potential and single neuron encoding of reward-based decisions

Abstract

Reward-guided behaviors require functional interaction between amygdala, orbital (OFC), and medial (MFC) divisions of prefrontal cortex, but the neural mechanisms underlying these interactions are unclear. Here, we used a decoding approach to analyze local field potentials (LFPs) recorded from OFC and MFC of monkeys engaged in a stimulus-choice task, before and after excitotoxic amygdala lesions. Whereas OFC LFP responses were strongly modulated by the amount of reward associated with each stimulus, MFC responses best represented which stimulus subjects decided to choose. This was counter to what we observed in the level of single neurons where their activity was closely associated with the value of the stimuli presented on each trial. After lesions of the amygdala, stimulus-reward value and choice encoding were reduced in OFC and MFC, respectively. However, while the lesion-induced decrease in OFC LFP encoding of stimulus-reward value mirrored changes in single neuron activity, reduced choice encoding in MFC LFPs was distinct from changes in single neuron activity. Thus, LFPs and single neurons represent different information required for decision-making in OFC and MFC. At the circuit-level, amygdala input to these two areas play a distinct role in stimulus-reward encoding in OFC and choice encoding in MFC.

Dissociable representations of decision variables within subdivisions of macaque orbitofrontal and ventrolateral frontal cortex

“…Altogether, we found that many neurons across ventral frontal cortex represented the chosen flavor and probability of the outcomes that would follow a specific stimulus, further supporting the involvement of this part of frontal cortex in the valuation stage of decision making (Noonan et al, 2017;Murray and Rudebeck, 2018;Stoll and Rudebeck, 2023). Representations were, however, not uniform across subdivisions and were dissociable based on encoding and decoding approaches.…”

“…Numerous prior reports have shown that neurons across frontal cortex often exhibit "mixed selectively" in that they code for multiple task features (Rigotti et al, 2013;Fusi et al, 2016). We and others previously reported that vlPFC and OFC neurons are highly likely to exhibit mixed selectivity while maintaining orthogonal representations of the factors important for valuation (for instance, (Wallis and Miller, 2003;Stoll and Rudebeck, 2023). To establish if there were any differences in the degree of mixed selectivity between subdivisions of ventral frontal cortex, we conducted a similar set of analyses here.…”

“…Raw electrophysiological activity was recorded using an Omniplex data acquisition system (Plexon, Dallas, TX) and sampled at a 40kHz resolution. Spikes from putative single neurons were automatically clustered offline using the MountainSort plugin of MountainLab (Chung et al, 2017) and later curated manually based on the principal component analysis, interspike interval distributions, visually differentiated waveforms, and objective cluster measures (Isolation > 0.75, Noise overlap < 0.2, Peak signal to noise ratio > 0.5, Firing Rate > 0.05 Hz) (Stoll and Rudebeck, 2023).…”

“…Monkeys were trained to perform 3 closely related tasks during each session, including a Single option, Instrumental and Dynamic probabilistic tasks (Stoll and Rudebeck, 2023). Our current analyses focused on instrumental trials only.…”

“…Prior work has highlighted a role for OFC in valuation processes, especially when subjects are making value-based decisions (Thorpe et al, 1983;Tremblay and Schultz, 1999;Padoa-Schioppa and Assad, 2006;Bouret and Richmond, 2010;Kobayashi et al, 2010;Rudebeck et al, 2013a;Pastor-Bernier et al, 2019;Stoll and Rudebeck, 2023).…”