Choice-Selective Neurons in the Auditory Cortex and in Its Striatal Target Encode Reward Expectation

Abstract

Learned behavioral responses to sounds depend largely on the expected outcomes associated with each potential choice. Where and how the nervous system integrates expectations about reward with auditory sensory information to drive appropriate decisions is not fully understood. Using a two-alternative choice task in which the expected reward associated with each sound varied over time, we investigated potential sites along the corticostriatal pathway for the integration of sound signals, behavioral choice, and reward information in male mice. We found that auditory cortical neurons encode not only sound identity, but also the animal's choice and the expected size of reward. This influence of reward expectation on sound-and choice-related activity was further enhanced in the major striatal target of the auditory cortex: the posterior tail of the dorsal striatum. These results indicate that choice-specific information is integrated with reward signals throughout the corticostriatal pathway, potentially contributing to adaptation in sound-driven behavior.

Learning-related population dynamics in the auditory thalamus

“…The medial and dorsal parts of the MGB are part of a thalamocortical loop that has been suggested to encode high-order cognitive information (Bolkan et al, 2017; Guo et al, 2017; Schmitt et al, 2017). Choice encoding in the thalamus (Chen et al, 2019; Gimenez et al, 2015; Jaramillo et al, 2014) bears similarity to previous observations in the cortex (Gilad et al, 2018; Guo et al, 2019; Harvey et al, 2012; Pho et al, 2018; Siegel et al, 2015; Yang et al, 2015), indicating the involvement of the thalamocortical loop during learning. Choice encoding was consistent across mice and evident at the population level.…”

“…This simultaneous change in activity and learning is similar to the observed change in cortical areas (Gilad and Helmchen, 2019) and may indicate a tight relation between learning, thalamus and cortex. Our results imply that choice information may already originate in MGB, which is then relayed to the auditory cortex (Guo et al, 2019). Alternatively, the MGB may be activated via the thalamocortical loop with auditory cortex.…”

“…For example, neural signals in animals that gain expertise in a specific task, show increased activity and result in higher discriminatory power between the learned stimuli (Gilad et al, 2018; Gilad and Helmchen, 2019; Poort et al, 2015; Wiest et al, 2010; Yan et al, 2014). In the auditory system, when training to discriminate between two sounds, neurons in auditory cortex display several learning related modulations: encoding of higher-order choice information (Guo et al, 2019; Jaramillo et al, 2014), tonotopic map reorganization (Maor et al, 2020; Polley et al, 2006), increased responses to a target frequency and decreased responses to a distractor stimulus (Blake et al, 2002; David et al, 2012; Ghose, 2004; Ohl and Scheich, 2005). In addition, a large body of evidence indicates that the medial MGB is involved in auditory fear conditioning, by providing fast, less refined auditory information to the lateral amygdala (Han et al, 2008; Herry and Johansen, 2014; Maren and Quirk, 2004; Quirk et al, 1995; Romanski and LeDoux, 1992; Weinberger, 2011), an indication of experience dependent synaptic plasticity in the MGB.…”

Becoming a better parent: mice learn sounds that improve a stereotyped maternal behavior

“…Our pup-predictive sound was presented from the left or right side at the decision point, and prior studies suggest that auditory cortical activity is not needed to localize the hemisphere from which a long duration sound is played [33,34]. On the other hand, the necessity of auditory cortical activity 475 for accurately choosing an arm to search, despite other auditory pathways for influencing behavioral responses to sounds [35], is consistent with auditory cortical projections affecting behavioral choices in sound-based tasks [36,37].…”

Task-induced modulations of neuronal activity along the auditory pathway

“…The response of sensory neurons can be modulated not only by external factors such as the statistics of the environment (Simoncelli and Olshausen, 2001), but also by the internal state of the animal, and the auditory system is no exception (Busse et al, 2017;Kuchibhotla and Bathellier, 2018;Poulet and Crochet, 2019). The activity of auditory neurons has indeed been shown to be influenced by several task-related variables such as attention or engagement (Atiani et al, 2009;Francis et al, 2018b;Fritz et al, 2003;Kato et al, 2015;Kuchibhotla et al, 2017;Otazu et al, 2009;Yao et al, 2019), arousal (Lin et al, 2019;McGinley et al, 2015), movement (Bigelow et al, 2019;McGinley et al, 2015;Nelson and Mooney, 2016;Nelson et al, 2013;Schneider et al, 2014b;Williamson et al, 2015;Zhou et al, 2014), or reward (Brosch et al, 2011;Gruters and Groh, 2012;Guo et al, 2019;Komura et al, 2001;Metzger et al, 2006). However, these task-induced modulations have been usually investigated separately, and it is not clear to what extent these signals are concurrently broadcasted throughout the auditory system or if they are selectively targeted to specific neural subpopulations.…”