Prefrontal Neurons Predict Choices during an Auditory Same-Different Task

Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, NH 03755, USA.
Current Biology (Impact Factor: 9.92). 10/2008; 18(19):1483-8. DOI: 10.1016/j.cub.2008.08.054
Source: PubMed

ABSTRACT The detection of stimuli is critical for an animal's survival [1]. However, it is not adaptive for an animal to respond automatically to every stimulus that is present in the environment [2-5]. Given that the prefrontal cortex (PFC) plays a key role in executive function [6-8], we hypothesized that PFC activity should be involved in context-dependent responses to uncommon stimuli. As a test of this hypothesis, monkeys participated in a same-different task, a variant of an oddball task [2]. During this task, a monkey heard multiple presentations of a "reference" stimulus that were followed by a "test" stimulus and reported whether these stimuli were the same or different. While they participated in this task, we recorded from neurons in the ventrolateral prefrontal cortex (vPFC; a cortical area involved in aspects of nonspatial auditory processing [9, 10]). We found that vPFC activity was correlated with the monkeys' choices. This finding demonstrates a direct link between single neurons and behavioral choices in the PFC on a nonspatial auditory task.

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    • "Beyond the auditory cortex, do latter processing stages (e.g., the monkey ventral prefrontal cortex and human inferior frontal cortex) process categories for even more complex sounds? A reexamination of previous findings from our lab (Russ et al., 2008b; Tsunada et al., 2011) indicated important differences in neural categorization between the lateral belt and the ventral prefrontal cortex (Figure 3). We found that, at the population level, the category sensitivity for speech sounds in the prefrontal cortex was weaker than that in the lateral belt although neural activity in the prefrontal cortex transmitted a significant amount of categorical information. "
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    ABSTRACT: Categorization enables listeners to efficiently encode and respond to auditory stimuli. Behavioral evidence for auditory categorization has been well documented across a broad range of human and non-human animal species. Moreover, neural correlates of auditory categorization have been documented in a variety of different brain regions in the ventral auditory pathway, which is thought to underlie auditory-object processing and auditory perception. Here, we review and discuss how neural representations of auditory categories are transformed across different scales of neural organization in the ventral auditory pathway: from across different brain areas to within local microcircuits. We propose different neural transformations across different scales of neural organization in auditory categorization. Along the ascending auditory system in the ventral pathway, there is a progression in the encoding of categories from simple acoustic categories to categories for abstract information. On the other hand, in local microcircuits, different classes of neurons differentially compute categorical information.
    Frontiers in Neuroscience 06/2014; 8:161. DOI:10.3389/fnins.2014.00161 · 3.70 Impact Factor
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    • "However, given the general role of the PFC in executive function (Miller and Cohen, 2001), we posit that examining vPFC activity during such passive-listening tasks is not an appropriate assay of the computations that occur in this brain region. Instead, when vPFC activity is examined during active behavioral tasks or more complex stimulus-presentation paradigms, it becomes clear that vPFC activity is involved in those functions that utilize vocalization information (and other auditory signals) to help guide goaldirected behaviors, including those behaviors that require nonspatial attention, working memory, decision-making, and abstract categorization (Gifford et al., 2005; Plakke et al., 2013a,b, 2012; Poremba et al., 2013; Russ et al., 2008a). "
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    ABSTRACT: A listener's capacity to discriminate between sounds is related to the amount of acoustic variability that exists between these sounds. However, a full understanding of how this natural variability impacts neural activity and behavior is lacking. Here, we tested monkeys' ability to discriminate between different utterances of vocalizations from the same acoustic class (i.e., coos and grunts), while neural activity was simultaneously recorded in the anterolateral belt region (AL) of the auditory cortex, a brain region that is a part of a pathway that mediates auditory perception. Monkeys could discriminate between coos better than they could discriminate between grunts. We also found AL activity was more informative about different coos than different grunts. This difference could be attributed, in part, to our finding that coos had more acoustic variability than grunts. Thus, intrinsic acoustic variability constrained the discriminability of AL spike trains and the ability of rhesus monkeys to discriminate between vocalizations.
    Hearing research 04/2014; 312. DOI:10.1016/j.heares.2014.03.007 · 2.85 Impact Factor
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    • "These categories are represented in the ventral prefrontal cortex. Importantly, neural activity in the prefrontal cortex during categorization also predicts behavioral choice (Russ et al., 2008). Earlier in the stimulus-behavior transformation, these categories are differentially represented between interneurons and pyramidal neurons in the belt region of the auditory cortex (Tsunada et al., 2012), but this belt activity is not modulated by the monkey's categorical choices (Tsunada et al., 2011). "
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    ABSTRACT: Acoustic communication between animals requires them to detect, discriminate, and categorize conspecific or heterospecific vocalizations in their natural environment. Laboratory studies of the auditory-processing abilities that facilitate these tasks have typically employed a broad range of acoustic stimuli, ranging from natural sounds like vocalizations to "artificial" sounds like pure tones and noise bursts. However, even when using vocalizations, laboratory studies often test abilities like categorization in relatively artificial contexts. Consequently, it is not clear whether neural and behavioral correlates of these tasks (1) reflect extensive operant training, which drives plastic changes in auditory pathways, or (2) the innate capacity of the animal and its auditory system. Here, we review a number of recent studies, which suggest that adopting more ethological paradigms utilizing natural communication contexts are scientifically important for elucidating how the auditory system normally processes and learns communication sounds. Additionally, since learning the meaning of communication sounds generally involves social interactions that engage neuromodulatory systems differently than laboratory-based conditioning paradigms, we argue that scientists need to pursue more ethological approaches to more fully inform our understanding of how the auditory system is engaged during acoustic communication.
    Hearing research 08/2013; 305(1). DOI:10.1016/j.heares.2013.08.008 · 2.85 Impact Factor
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