Oxford Handbook of Auditory Science The Auditory Brain
Adrian Rees Institute of Neuroscience
Alan R. Palmer MRC Institute of Hearing Research
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Emotional responses to auditory stimuli
Jorge L. Armony and Joseph E. LeDoux
19.1 Introduction The ability to quickly detect and accurately decode emotional stimuli arising in the environment is critical for an organisms survival. Some of these stimuli are species-specific and their affective value innate, genetically determined throughout evolution. In contrast, other signals have no intrinsic meaning and only acquire a particular emotional value through experience; their mean-ing may thus vary from individual to individual, and depends on the specific spatial and temporal context in which they appear. Although all sensory modalities can carry emotional information, acoustic stimuli are particularly well suited for efficiently conveying biologically relevant infor-mation, such as information about predators. For instance, the sound made by an approaching predator can be detected well before the animal enters the potential preys field of view. This is due to the ability of auditory stimuli to signal distant events and their rapid transmission through the nervous system. However, acoustic signals are also useful in communicating between members of a species. In both human and non-human species, vocalizations are relied upon extensively in intra-species communication. In spite of the necessity of the sensory systems in processing biologically significant stimuli, emotional meaning requires that processing extend beyond the traditional sensory systems to structures such as the amygdala.
In this chapter, we describe what is currently known about the neural structures and mecha-nisms associated with the processing of emotional auditory information for stimuli with intrinsic or learned affective value. We focus on the amygdala, as this structure has been consistently shown to be a crucial component of the emotional brain, across several sensory modalities, in particular, within the auditory domain.
19.2 Fear conditioning Most of what is known about the neural bases and mechanisms of auditory emotional processing has been learned through the use of aversive classical or Pavlovian conditioning. In this paradigm, also referred to as fear conditioning, an emotionally neutral stimulus (the conditioned stimulus; CS), such as a simple tone, is paired with an intrinsically noxious stimulus (the unconditioned stimulus; US), such as a mild electric shock, which elicits unconditioned defensive responses. Before conditioning, the CS does not elicit any overt behavioral reaction (except an initial orient-ing response). However, after a few pairings, sometimes as little as one, an association between the conditioned and unconditioned stimuli is formed, such that when the CS is presented alone, the individual will now exhibit a host of species-specific conditioned fear responses. That is, through conditioning, new stimuli that become warning signals for impending threat can gain access to evolutionary shaped defensive responses, allowing the individual to rapidly respond to, or even avoid, the dangerous situation.
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JORGE L. ARMONY AND JOSEPH E. LEDOUX478
In rats, conditioned fear responses include freezing (i.e., absence of any movement except those associated with breathing), vocalizations, increase of heart rate, blood pressure, defecation, and the potentiation of reflexes such as the acoustic startle response (Blanchard and Blanchard, 1969 ; Kapp et al ., 1979 ; LeDoux et al ., 1988 ; Davis, 1992 ; Borszcz, 1995 ). In humans, some of the conditioned responses that are typically measured are muscle tension, pupil dilation, changes in heart rate, blood pressure, respiration and, most often, electrodermal or skin conductance responses, which are mediated by the sympathetic nervous system.
Fear conditioning not only is a powerful paradigm to study the neurobiology of emotional processing and learning in the healthy brain, but also has been proposed as a model to account, at least in part, for some of the key features associated with the development of certain psychiatric disorders involving a dysregulation of the fear system, such as phobias and post-traumatic stress disorder (Davis, 1992 ; Armony and LeDoux, 1997 ; Rasmusson and Charney, 1997 ; Brewin, 2001 ).
19.2.1 Neural circuits There is a large body of literature pointing towards the amygdala as a critical structure for auditory fear conditioning. Disruption of this structure by permanent lesions or temporary inactivation disrupts the learning of the CSUS association and hence the development of conditioned fear. Interestingly, while bilateral lesions completely abolish conditioning, unilateral lesions result in a substantial, though partial, reduction of fear responses to the CS, with no significant differences between lesions in the right or left hemispheres (LaBar and LeDoux, 1996 ; Baker and Kim, 2004 ).
The amygdala is a relatively heterogeneous conglomerate of cells located in the depth of the anteromedial temporal lobe. Although there is still no consensus on its exact borders or the nomenclature of its nuclei, most researchers now agree that the amygdala is composed of about a dozen nuclei, each of them in turn subdivided into several subregions with unique architectonic, histochemical, and physiological characteristics (Pitkanen, 2000 ; De Olmos, 2004 ). The main features of the amygdala appear to have been highly conserved throughout evolution. Indeed, its basic structure and function is strikingly similar across mammals, including rodents, monkeys, and humans ( Fig. 19.1 ). In fact, it has been suggested that other species, such as birds (Lowndes and Davies, 1994 ) and fish (Portavella et al ., 2004 ), also have amygdala-like structures which mediate some aspect of their emotional behavior, in particular the acquisition and expression of conditioned fear responses.
An acoustic CS is transmitted from cochlear receptors through the brainstem to the auditory thalamus, the medial geniculate body (MGB). Information is then conveyed to the amygdala by way of two parallel routes (LeDoux, 1996 ). A direct projection originates primarily in the medial division of the MGB (MGm) and the associated posterior intralaminar nucleus (PIN). A second, indirect pathway involves projections from all areas of the MGB to the auditory cortex, from where, via several cortico-cortical links, information about the CS reaches the amygdala (see Fig. 19.2 ).
Both pathways terminate primarily in the lateral nuc