Parallel lemniscal and non-lemniscal sources control auditory responses in the orbitofrontal cortex (OFC)

The orbitofrontal cortex (OFC), controls flexible behavior through stimulus value updating based on stimulus outcome associations, allowing seamless navigation in dynamic sensory environments with changing contingencies. Sensory cue driven responses, primarily studied through behavior, exist in the OFC. However, OFC neurons’ sensory response properties, particularly auditory, are unknown, in the mouse, a genetically tractable animal. We show that mouse OFC single neurons have unique auditory response properties showing pure deviance detection and long timescales of adaptation resulting in stimulus-history dependence. Further, we show that OFC auditory responses are shaped by two parallel sources in the auditory thalamus, lemniscal and non-lemniscal. The latter underlies a large component of the observed deviance detection and additionally controls persistent activity in the OFC through the amygdala. The deviant selectivity can serve as a signal for important changes in the auditory environment. Such signals if coupled with persistent activity, obtained by disinhibitory control from the non-lemniscal auditory thalamus or the amygdala, will allow for associations with a delayed outcome related signal, like reward prediction error, and potentially forms the basis of updating stimulus outcome associations in the OFC. Thus the baseline sensory responses allow the behavioral requirement based response modification through relevant inputs from other structures related to reward, punishment, or memory. Thus, alterations in these responses in neurological disorders can lead to behavioral deficits.

Quantitative Assessment of the Timing and Tuning of Visual-Related, Saccade-Related, and Delay Period Activity in Primate Central Thalamus

This study investigates the visuomotor properties of several nuclei within primate central thalamus. These nuclei, which might be considered components of an oculomotor thalamus (OcTh), are found within and at the borders of the internal medullary lamina. These nuclei have extensive anatomical links to numerous cortical and subcortical visuomotor areas including the frontal eye fields, supplementary eye fields, prefrontal cortex, posterior parietal cortex, caudate, and substantia nigra pars reticulata. Previous single-unit recordings have shown that neurons in OcTh respond during self-paced spontaneous saccades and to visual stimuli in the absence of any specific behavioral requirement, but a thorough account of the activity of these areas in association with voluntary, goal-directed movement is lacking. We recorded activity from single neurons in primate central thalamus during performance of a visually guided delayed saccade task. The sample consisted primarily of neurons from the centrolateral and paracentral intralaminar nuclei and paralaminar regions of the ventral anterior and ventral lateral nuclei. Neurons responsive to sensory, delay, and motor phases of the task were observed in each region, with many neurons modulated during multiple task periods. Across the population, variation in the quality and timing of saccade-contingent activity suggested participation in functions ranging from generating a saccade (presaccadic) to registering its consequences (e.g., efference copy). Finally, many neurons were found to carry spatial information during the delay period, suggesting a role for central thalamus in higher-order aspects of visuomotor control.