Elsevier

Neuroscience

Volume 299, 23 July 2015, Pages 45-55
Neuroscience

Neuroscience Forefront Review
Auditory cortex involvement in emotional learning and memory

https://doi.org/10.1016/j.neuroscience.2015.04.068Get rights and content

Highlights

  • New vistas on sensory cortex involvement in emotional learning.

  • Primary and higher order cortices are essential for emotional learning.

  • Sensory cortices store affectively laden memories.

Abstract

Emotional memories represent the core of human and animal life and drive future choices and behaviors. Early research involving brain lesion studies in animals lead to the idea that the auditory cortex participates in emotional learning by processing the sensory features of auditory stimuli paired with emotional consequences and by transmitting this information to the amygdala. Nevertheless, electrophysiological and imaging studies revealed that, following emotional experiences, the auditory cortex undergoes learning-induced changes that are highly specific, associative and long lasting. These studies suggested that the role played by the auditory cortex goes beyond stimulus elaboration and transmission. Here, we discuss three major perspectives created by these data. In particular, we analyze the possible roles of the auditory cortex in emotional learning, we examine the recruitment of the auditory cortex during early and late memory trace encoding, and finally we consider the functional interplay between the auditory cortex and subcortical nuclei, such as the amygdala, that process affective information. We conclude that, starting from the early phase of memory encoding, the auditory cortex has a more prominent role in emotional learning, through its connections with subcortical nuclei, than is typically acknowledged.

Introduction

During emotional experiences, sensory stimuli such as sounds, odors and colors acquire a positive or negative value through their association with rewards or punishments, respectively, in a process called “emotional learning”. Emotional learning is typically studied in animals, including humans, using classical pavlovian conditioning; in this procedure, a subject is exposed to a conditioned stimulus (CS), such as a tone, light or odor, in association with an unconditioned stimulus (US). Depending on the type of US, there are two main forms of pavlovian conditioning. In appetitive conditioning, the US is a positive reinforcement such as food, drink or addictive drug. In aversive conditioning, the US is an unpleasant deterrent such as a foot shock, loud noise or air puff. In both appetitive and aversive conditioning, following pairing of the CS with the US, the CS takes on the affective qualities of the US and later, in the absence of the US, it will evoke a conditioned emotional reaction.

The memory of past emotional and sensory events is encoded, at least in part, in the sensory cortex. Early attempts to identify the neural circuitry underlying emotional learning found that lesions in the auditory or visual cortex of rodents did not prevent the formation of auditory or visual memories of fear (LeDoux et al., 1989, Romanski and LeDoux, 1992a, Romanski and LeDoux, 1992b, Falls and Davis, 1993). Moreover, these lesions did not affect the retention of auditory or visual fear memories when they were made shortly after training (Jarrell et al., 1987, Rosen et al., 1992, Campeau and Davis, 1995). Romanski and LeDoux (1992b) compared the effects of lesions in the thalamo-cortico-amygdala projection and in the thalamo-amygdala projection: destruction of either pathway alone had no effect on auditory fear conditioning, while combined lesions in both sensory pathways disrupted it. These data led to the standard hypothesis, which states that sensory inputs to the amygdala come from both the thalamus and the sensory cortex and that fear conditioning to a simple auditory stimulus (“cued fear conditioning”) can be mediated by either of these pathways (LeDoux, 2000). More recently, however, Boatman and Kim found that lesions in the thalamo-amygdala projection caused severe but incomplete deficits in the retention of auditory fear memories, while lesions in the thalamo-cortico-amygdala connectivity abolished it completely; these authors therefore suggested that the thalamo-cortico-amygdala route is the principal pathway for auditory fear learning in intact rat brain (Boatman and Kim, 2006).

Altogether, these lesion studies lead to the idea that the auditory cortex is dispensable for emotional memory formation and retrieval. However, electrophysiological studies have provided evidence for learning-induced plasticity in the auditory cortex that transcends the analysis of physical properties of auditory stimuli and their transmission to the amygdala. Auditory cortical plasticity has been reported in animal models and for both appetitive and aversive conditioning (see Weinberger, 2004, Weinberger, 2007, Weinberger, 2015, Ohl and Scheich, 2005, Brosch et al., 2011a for extensive reviews). Furthermore, evidence of learning-evoked plasticity in the human auditory cortex has been provided by neuroimaging studies using PET (Molchan et al., 1994, Morris et al., 1998), functional MRI (Thiel et al., 2002), and magnetoencephalography (Kluge et al., 2011). Plasticity in the auditory cortex was strictly related to learning processes, in both humans and animals. Furthermore, it developed rapidly and became stronger over days without further training, lasting up to 8 weeks in rodents (Weinberger, 2004, Weinberger, 2007, Weinberger, 2015). These findings are at odds with the previously mentioned lesion studies. As a consequence, despite more than 30 years of research, the roles and conditions of auditory cortex involvement in emotional processing remain largely controversial. In this Forefront Review, we discuss: (i) the roles of the auditory cortex in emotional learning and memory processing, (ii) the dynamics of auditory cortex recruitment during the course of emotional memory formation, consolidation and storage, and (iii) the functional interplay between the auditory cortex and subcortical nuclei, specifically the amygdala and striatum, during memory encoding and retrieval.

Section snippets

Roles of the auditory cortex in emotional learning and memory processing

Emotional learning involves several processes: the elaboration and subsequent memorization of the sensory features of the CS and US (“perceptual learning”); the linking of different sensory stimuli (“S–S learning”); and the association of the CS to the value of (or the response to) the US. The most commonly employed learning paradigms, such as fear conditioning and appetitive conditioning, engage these processes simultaneously and thus do not allow them to be studied separately. Furthermore,

Auditory cortex and the formation of recent and remote emotional memories

Memories are thought to require a prolonged consolidation process in order to be stabilized and maintained for weeks, months and years (McGaugh, 2000, McGaugh, 2015, Frankland and Bontempi, 2005). Memory consolidation involves reorganization at the synaptic and system levels. Synaptic consolidation is based on changes in synaptic architecture, whereas consolidation at the system level involves changes in the neural circuits that support memory. The standard theory of system-level memory

Functional interplay between the auditory cortex and the subcortical structures

Subcortical nuclei, such as the amygdala and striatum, are fundamental for the processing of affective information. These structures are reciprocally connected to the auditory cortex (Kolb and Tees, 1990, Amaral et al., 1992, Romanski and LeDoux, 1993, Paxinos, 2004); thus these brain areas may interact in the course of emotional memory encoding. Nevertheless, the direction of the information flux between the auditory cortex and these subcortical nuclei may vary during the acquisition and

Conclusions

Our understanding of the neuroanatomy of emotional learning, especially fear learning, has evolved substantially from the early theories developed in the 1980s. Initially, the amygdala was considered a key node, whereas the auditory cortex was considered mostly a CS analyzer that transmitted sensory information to the amygdala, especially for more complex auditory stimuli (reviewed in LeDoux, 2000). Starting in the mid-1980s, Scheich and colleagues (Ohl and Scheich, 2005, Brosch et al., 2011a)

Acknowledgements

We are grateful to A. Renna and L. Milano (University of Turin, Turin, Italy) for critical comments on the manuscript and for their continuous support and advice. We also thank V. Matarese for the critical reading and editing of the manuscript. This work was supported by grants from the European Research Council (ERC) under the European Union’s Seventh Framework Program (FP7/2007-2013/ERC grant agreement no. 281072) and from the Compagnia di San Paolo, Progetto d’Ateneo, Università di Torino

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