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      Physiological differences between histologically defined subdivisions in the mouse auditory thalamus

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          Abstract

          The auditory thalamic area includes the medial geniculate body (MGB) and the lateral part of the posterior thalamic nucleus (Pol). The MGB can be subdivided into a ventral subdivision, forming part of the lemniscal (primary) auditory pathway, and medial and dorsal subdivisions, traditionally considered (alongside the Pol) part of the non-lemniscal (secondary) pathway. However, physiological studies of the auditory thalamus have suggested that the Pol may be more appropriately characterised as part of the lemniscal pathway, while the medial MGB may be part of a third (polysensory) pathway, with characteristics of lemniscal and non-lemniscal areas. We document physiological properties of neurons in histologically identified areas of the MGB and Pol in the anaesthetised mouse, and present evidence in favour of a distinctive role for medial MGB in central auditory processing. In particular, medial MGB contains a greater proportion of neurons with short first-spike latencies and high response probabilities than either the ventral or dorsal MGB, despite having low spontaneous rates. Therefore, medial MGB neurons appear to fire more reliably in response to auditory input than neurons in even the lemniscal, ventral subdivision. Additionally, responses in the Pol are more similar to those in the ventral MGB than the dorsal MGB.

          Highlights

          ► We compared subdivisions of medial geniculate body and posterior thalamic nucleus. ► Latencies were shortest in medial subdivision, longest in dorsal subdivision. ► Response probability was highest in medial and ventral subdivisions. ► Some ventral subdivison and posterior thalamic neurons showed late “rebound” firing. ► Results support tripartite organisation of ascending auditory pathways.

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          Most cited references59

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          Stimulus-specific adaptation occurs in the auditory thalamus.

          Neurons in the primary auditory cortex respond less strongly to a commonly occurring "standard" tone than to the same tone when it is rare or "deviant." This phenomenon, called "stimulus-specific adaptation" (SSA), has been proposed as a possible single-neuron correlate of the mismatch negativity, a cortical evoked potential associated with stimulus novelty. Previous studies in cat did not observe SSA in single neurons in the auditory thalamus. However, these reports did not differentiate between the auditory thalamic subdivisions and did not examine the effects of changing the stimulus presentation rate. To explore the possibility of thalamic SSA more completely, we recorded extracellularly from 30 single units and 22 multiunit clusters in the ventral, medial, and dorsal subdivisions of the mouse medial geniculate body (MGB), while presenting the anesthetized animals with sequences of standard and deviant tones at interstimulus intervals of 400, 500 and 800 ms. We found SSA in the auditory thalamus at all three stimulus presentation rates, primarily in the medial subdivision but to a lesser degree also in the ventral MGB. Thalamic SSA was evident from the earliest onset of tone-evoked activity, although the latencies of responses to standard and deviant tones were not significantly different. Together with related findings of SSA in neurons of the "belt" regions of the inferior colliculus, these results demonstrate that SSA is present at subcortical levels, primarily in but not restricted to the nonlemniscal auditory pathway.
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            Retrospective and prospective coding for predicted reward in the sensory thalamus.

            Reward is important for shaping goal-directed behaviour. After stimulus-reward associative learning, an organism can assess the motivational value of the incoming stimuli on the basis of past experience (retrospective processing), and predict forthcoming rewarding events (prospective processing). The traditional role of the sensory thalamus is to relay current sensory information to cortex. Here we find that non-primary thalamic neurons respond to reward-related events in two ways. The early, phasic responses occurred shortly after the onset of the stimuli and depended on the sensory modality. Their magnitudes resisted extinction and correlated with the learning experience. The late responses gradually increased during the cue and delay periods, and peaked just before delivery of the reward. These responses were independent of sensory modality and were modulated by the value and timing of the reward. These observations provide new evidence that single thalamic neurons can code for the acquired significance of sensory stimuli in the early responses (retrospective coding) and predict upcoming reward value in the late responses (prospective coding).
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              Auditory thalamocortical transformation: structure and function.

              Communicative, predatory, and reproductive behaviors rely on the auditory thalamocortical system, a key nexus that combines, transforms, and distributes virtually all acoustic information relevant to survival. The rules of connectivity for this complex network, both anatomically and functionally, are only beginning to be uncovered. Although the auditory thalamocortical system shares many features with other modalities, its connectivity and information processing principles differ from those of other modalities in many ways. Some physiological and anatomical bases for these differences are the subject of this review.
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                Author and article information

                Journal
                Hear Res
                Hear. Res
                Hearing Research
                Elsevier/North-Holland Biomedical Press
                0378-5955
                1878-5891
                April 2011
                April 2011
                : 274
                : 1-2
                : 48-60
                Affiliations
                [a ]Ear Institute, University College London, London WC1X 8EE, UK
                [b ]Department of Neuroscience, Physiology & Pharmacology, University College London, London WC1E 6BT, UK
                Author notes
                []Corresponding author. UCL Ear Institute, 332 Gray’s Inn Road, London WC1X 8EE, UK. Tel.: +44 0207 679 8928; fax: +44 0207 679 8990. j.linden@ 123456ucl.ac.uk
                Article
                HEARES6282
                10.1016/j.heares.2010.12.016
                3078334
                21185928
                c71aa363-fc53-4fb3-82ba-8a576bc0fe06
                © 2011 Elsevier B.V.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 25 June 2010
                : 9 December 2010
                : 20 December 2010
                Categories
                Research Paper

                Audiology
                apt, anterior pretectal nucleus,psth, post-stimulus time histogram,cf, characteristic frequency,mgb, medial geniculate body,lgn, lateral geniculate nucleus,pol, lateral part of the posterior thalamic nucleus,cyo, cytochrome oxidase

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