Neural Estimates of Imagined Outcomes in Basolateral Amygdala Depend on Orbitofrontal Cortex

Abstract

Reciprocal connections between the orbitofrontal cortex (OFC) and the basolateral nucleus of the amygdala (BLA) provide a critical circuit for guiding normal behavior when information about expected outcomes is required. Recently, we reported that outcome signaling by OFC neurons is also necessary for learning in the face of unexpected outcomes during a Pavlovian over-expectation task. Key to learning in this task is the ability to build on prior learning to infer or estimate an amount of reward never previously received. OFC was critical to this process. Notably, in parallel work, we found that BLA was not necessary for learning in this setting. This suggested a dissociation in which the BLA might be critical for acquiring information about the outcomes but not for subsequently using it to make novel predictions. Here we evaluated this hypothesis by recording single-unit activity from BLA in rats during the same Pavlovian over-expectation task used previously. We found that spiking activity recorded in BLA in control rats did reflect novel outcome estimates derived from the integration of prior learning, however consistent with a model in which this process occurs in the OFC, these correlates were entirely abolished by ipsilateral OFC lesions. These data indicate that this information about these novel predictions is represented in the BLA, supported via direct or indirect input from the OFC, even though it does not appear to be necessary for learning.

Back to basics: Making predictions in the orbitofrontal–amygdala circuit

“…In particular, recent evidence suggests that signaling from the OFC contributes to the ability of neurons in the BLA to reflect the integration of information from multiple sources (Lucantonio, Gardner, Mirenzi, Newman, Takahashi, and Schoenbaum, 2015). In this study, rats were trained on an over-expectation task and neurons in the BLA were recorded in OFC-lesioned and sham-lesioned animals.…”

Inhibitory modulation of medial prefrontal cortical activation on lateral orbitofrontal cortex–amygdala information flow

“…), and the BLA loses its capability in integrating and updating information from multiple cue–outcome associations if the lOFC is damaged (Lucantonio et al . ). Another major input is from the medial prefrontal cortex (mPFC), both the prelimbic and the infralimbic divisions (Sotres‐Bayon & Quirk, ), which is critical for processing of emotional reactions.…”

“…; Rempel‐Clower, ), which is related to the development of cue–outcome contingencies (Schoenbaum & Roesch, ; Lucantonio et al . ; Sharpe & Schoenbaum, ). For example, reversal learning is facilitated by the lOFC (Schoenbaum et al .…”

“…One of the major inputs is from the lateral orbitofrontal cortex (lOFC) (Lopatina et al 2015), both the lateral orbital cortex (LO) and the agranular insula (AI; ventral and dorsal divisions) (Aggleton et al 1980;McDonald et al 1996;Rempel-Clower, 2007), which is related to the development of cue-outcome contingencies (Schoenbaum & Roesch, 2005;Lucantonio et al 2015;Sharpe & Schoenbaum, 2016). For example, reversal learning is facilitated by the lOFC (Schoenbaum et al 2007;Ghods-Sharifi et al 2008), and the BLA loses its capability in integrating and updating information from multiple cue-outcome associations if the lOFC is damaged (Lucantonio et al 2015). Another major input is from the medial prefrontal cortex (mPFC), both the prelimbic and the infralimbic divisions (Sotres-Bayon & Quirk, 2010), which is critical for processing of emotional reactions.…”

Dano seletivo no córtex orbitofrontal em ratos não interfere na aquisição de uma tarefa de escolha intertemporal nem no seu desempenho quando adquirida previamente a lesão

“…A partir da emissão do valor, o indivíduo opta por uma escolha supostamente mais vantajosa e, assim, direciona suas ações com base no princípio de que deve-se maximizar a obtenção de benefícios. As escolhas vantajosas são as que atenderiam aos requisitos de menor esforço, menor tempo de espera, maior qualidade ou quantidade, ao contrário das que possuam maior esforço, maior tempo de espera e menor quantidade e qualidade (BASTEN et al, 2010;TSE;GHODS-SHARIFI, 2008;KABLE;GLIMCHER, 2009;LUCANTONIO et al, 2015;RUSHWORTH et al, 2011).…”