The Basal Forebrain Modulates Neuronal Response in an Active Olfactory Discrimination Task.

Alexia Nunez-Parra,Diego Restrepo,Molly M Huntsman,Christian A Cea-Del Rio

doi:10.3389/fncel.2020.00141

Abstract

Successful completion of sensory decision-making requires focusing on relevant stimuli, adequate signal/noise ratio for stimulus discrimination, and stimulus valence evaluation. Different brain regions are postulated to play a role in these computations; however, evidence suggests that sensory and decision-making circuits are required to interact through a common neuronal pathway to elicit a context-adequate behavioral response. Recently, the basal forebrain (BF) region has emerged as a good candidate, since its heterogeneous projecting neurons innervate most of the cortical mantle and sensory processing circuits modulating different aspects of the sensory decision-making process. Moreover, evidence indicates that the BF plays an important role in attention and in fast modulation of neuronal activity that enhance visual and olfactory sensory perception. Here, we study in awake mice the involvement of BF in initiation and completion of trials in a reward-driven olfactory detection task. Using tetrode recordings, we find that BF neurons (including cholinergics) are recruited during sensory discrimination, reward, and interestingly slightly before trial initiation in successful discrimination trials. The precue neuronal activity was correlated with animal performance, indicating that this circuit could play an important role in adaptive context-dependent behavioral responses.

Highlights

Efficient sensory decision-making in a constantly changing environment requires neuronal circuits to be plastic and rapidly modify their activity
To study the dynamics of recruitment of basal forebrain (BF) neurons in animals engaged in a self-initiated decision-making task, we implanted a multielectrode device in the horizontal diagonal band of Broca/magnocellular preoptic (HDB/MCPO) nuclei and proximity in the BF of trained adult mice (Supplementary Figures S1A,B)
We found that the number of units responsive at port entry was significantly lower in the go/go task compared to the go/no–go task (Figure 1Eii and Supplementary Figure S2, chi-squared test p < pFDR = 0.05, go/no–go = 53 responsive out of 153 or 34.6%), go/go = 8 responsive out of 44 or 18.2%, all of which increased their firing rate (FR), suggesting that BF neuronal recruitment before trial initiation may play a role in adequate stimulus discrimination

Summary

Introduction

Efficient sensory decision-making in a constantly changing environment requires neuronal circuits to be plastic and rapidly modify their activity. The basal forebrain (BF) emerges as a good candidate to participate as an integrator and neuromodulator source for behavior since it is one of the most important and widely projecting neuromodulatory circuits in the mammalian brain (Gritti et al, 2006) reaching the entire cortical mantle, hippocampus, and the olfactory system among others (Luskin and Price, 1982; Zaborszky et al, 1986; Zaborszky, 2012). It has been linked with attention (Klinkenberg et al, 2011), arousal (Buzsaki et al, 1988), and learning and memory (Everitt and Robbins, 1997; Klinkenberg et al, 2011). Its subnuclei have been proposed to play important roles in components of goaldirected behaviors such as motivational saliency (Lin and Nicolelis, 2008), sensory discrimination (Lin and Nicolelis, 2008; Devore and Linster, 2012; Nunez-Parra et al, 2013; Pinto et al, 2013; Devore et al, 2016), and cortical control (Picciotto et al, 2012)

Methods

Results

Conclusion