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Characterizing spatial tuning functions of neurons in the auditory cortex of young and aged monkeys: a new perspective on old data.

Engle JR, Recanzone GH - Front Aging Neurosci (2013)

Bottom Line: It is also possible that spatial tuning was decreased as a consequence of reduced inhibition at non-best locations.In this report we found that aged animals had greater activity throughout the response period, but primarily during the onset of the response.These results can be interpreted in the context of a failure of the timing and efficiency of feed-forward thalamo-cortical and cortico-cortical circuits in aged animals.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology and Center for Neuroscience, University of California at Davis Davis, CA, USA ; Evelyn F. McKnight Brain Institute and ARL Division of Neural Systems, Memory and Aging, University of Arizona Tucson, AZ, USA.

ABSTRACT
Age-related hearing deficits are a leading cause of disability among the aged. While some forms of hearing deficits are peripheral in origin, others are centrally mediated. One such deficit is the ability to localize sounds, a critical component for segregating different acoustic objects and events, which is dependent on the auditory cortex. Recent evidence indicates that in aged animals the normal sharpening of spatial tuning between neurons in primary auditory cortex to the caudal lateral field does not occur as it does in younger animals. As a decrease in inhibition with aging is common in the ascending auditory system, it is possible that this lack of spatial tuning sharpening is due to a decrease in inhibition at different periods within the response. It is also possible that spatial tuning was decreased as a consequence of reduced inhibition at non-best locations. In this report we found that aged animals had greater activity throughout the response period, but primarily during the onset of the response. This was most prominent at non-best directions, which is consistent with the hypothesis that inhibition is a primary mechanism for sharpening spatial tuning curves. We also noted that in aged animals the latency of the response was much shorter than in younger animals, which is consistent with a decrease in pre-onset inhibition. These results can be interpreted in the context of a failure of the timing and efficiency of feed-forward thalamo-cortical and cortico-cortical circuits in aged animals. Such a mechanism, if generalized across cortical areas, could play a major role in age-related cognitive decline.

No MeSH data available.


Related in: MedlinePlus

Two parallel thalamo-cortical circuits to auditory cortex in young (left) and aged (right) monkeys. Simplified schematic diagram of the ventral and dorsal thalamo-cortical connections to the internal and supragranular layers in the macaque auditory system. The illustration in to lower aspect represents the three main subdivisions of the medial geniculate, the dorsal (D), ventral (V), and medial (mc) divisions. The ventral pathway is from the ventral division to the middle cortical layers of A1 (left) whereas the dorsal pathway initiates in the dorsal division and projects to the upper layers of both A1 and CL. A1 also projects directly to CL. Requiring coincidence of these two pathways is one mechanism by which spatial tuning could be sharpened in CL relative to A1 in young monkeys. In aged monkeys, the increase of activity in A1 and CL degrades with the cortical dynamics that sharpen spatial tuning in CL relative to A1. Abbrevations: V, ventral division of the MGN; D, dorsal division of the MGN; mc, medial division of the MGN; A1, primary auditory area; CL, caudolateral belt area.
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Figure 10: Two parallel thalamo-cortical circuits to auditory cortex in young (left) and aged (right) monkeys. Simplified schematic diagram of the ventral and dorsal thalamo-cortical connections to the internal and supragranular layers in the macaque auditory system. The illustration in to lower aspect represents the three main subdivisions of the medial geniculate, the dorsal (D), ventral (V), and medial (mc) divisions. The ventral pathway is from the ventral division to the middle cortical layers of A1 (left) whereas the dorsal pathway initiates in the dorsal division and projects to the upper layers of both A1 and CL. A1 also projects directly to CL. Requiring coincidence of these two pathways is one mechanism by which spatial tuning could be sharpened in CL relative to A1 in young monkeys. In aged monkeys, the increase of activity in A1 and CL degrades with the cortical dynamics that sharpen spatial tuning in CL relative to A1. Abbrevations: V, ventral division of the MGN; D, dorsal division of the MGN; mc, medial division of the MGN; A1, primary auditory area; CL, caudolateral belt area.

Mentions: This study was motivated by our desire to gain a better understanding of the neurophysiological correlates of the spatial processing deficits that have been reported in aged populations (Brown, 1984; Kubo et al., 1998; Abel et al., 2000), and to extend our recent findings that spatial tuning in area CL becomes degraded by normal aging (Juarez-Salinas et al., 2010). We studied both driven and inhibitory responses during different epochs of the response period to tease apart when in time the spatial tuning was degraded with age and explored whether a lack of inhibition of the parallel thalamic projections to the auditory cortex could account for changes in spatial tuning (Jones, 2003). A schematic of these pathways is shown in Figure 10, where CL neurons receive parallel input from both the dorsal thalamo-cortical pathway as well as serially from A1 [see also Rauschecker et al. (1997)]. Our results indicate that normal aging affects both pathways. They demonstrate that normal aging decreases the efficacy of inhibitory activity to regulate the neuronal response to sound from different locations in space and suggest that the tegmental thalamo-cortical pathway is normally suppressed in young animals. Population rate and latency codes of acoustic space were also impaired by normal aging, which resulted in an age-related change in the population's representation of acoustic space in azimuth (see Figure 3). This lack of inhibition is likely also responsible for the non-monotonic response as a function of time in the aged animals, particularly at nearby but non-best directions, as a function of time (see Figure 2). These results suggest that one of the main central effects of normal aging is the perturbation of the timing and efficacy of inhibition of auditory cortical responses.


Characterizing spatial tuning functions of neurons in the auditory cortex of young and aged monkeys: a new perspective on old data.

Engle JR, Recanzone GH - Front Aging Neurosci (2013)

Two parallel thalamo-cortical circuits to auditory cortex in young (left) and aged (right) monkeys. Simplified schematic diagram of the ventral and dorsal thalamo-cortical connections to the internal and supragranular layers in the macaque auditory system. The illustration in to lower aspect represents the three main subdivisions of the medial geniculate, the dorsal (D), ventral (V), and medial (mc) divisions. The ventral pathway is from the ventral division to the middle cortical layers of A1 (left) whereas the dorsal pathway initiates in the dorsal division and projects to the upper layers of both A1 and CL. A1 also projects directly to CL. Requiring coincidence of these two pathways is one mechanism by which spatial tuning could be sharpened in CL relative to A1 in young monkeys. In aged monkeys, the increase of activity in A1 and CL degrades with the cortical dynamics that sharpen spatial tuning in CL relative to A1. Abbrevations: V, ventral division of the MGN; D, dorsal division of the MGN; mc, medial division of the MGN; A1, primary auditory area; CL, caudolateral belt area.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3539457&req=5

Figure 10: Two parallel thalamo-cortical circuits to auditory cortex in young (left) and aged (right) monkeys. Simplified schematic diagram of the ventral and dorsal thalamo-cortical connections to the internal and supragranular layers in the macaque auditory system. The illustration in to lower aspect represents the three main subdivisions of the medial geniculate, the dorsal (D), ventral (V), and medial (mc) divisions. The ventral pathway is from the ventral division to the middle cortical layers of A1 (left) whereas the dorsal pathway initiates in the dorsal division and projects to the upper layers of both A1 and CL. A1 also projects directly to CL. Requiring coincidence of these two pathways is one mechanism by which spatial tuning could be sharpened in CL relative to A1 in young monkeys. In aged monkeys, the increase of activity in A1 and CL degrades with the cortical dynamics that sharpen spatial tuning in CL relative to A1. Abbrevations: V, ventral division of the MGN; D, dorsal division of the MGN; mc, medial division of the MGN; A1, primary auditory area; CL, caudolateral belt area.
Mentions: This study was motivated by our desire to gain a better understanding of the neurophysiological correlates of the spatial processing deficits that have been reported in aged populations (Brown, 1984; Kubo et al., 1998; Abel et al., 2000), and to extend our recent findings that spatial tuning in area CL becomes degraded by normal aging (Juarez-Salinas et al., 2010). We studied both driven and inhibitory responses during different epochs of the response period to tease apart when in time the spatial tuning was degraded with age and explored whether a lack of inhibition of the parallel thalamic projections to the auditory cortex could account for changes in spatial tuning (Jones, 2003). A schematic of these pathways is shown in Figure 10, where CL neurons receive parallel input from both the dorsal thalamo-cortical pathway as well as serially from A1 [see also Rauschecker et al. (1997)]. Our results indicate that normal aging affects both pathways. They demonstrate that normal aging decreases the efficacy of inhibitory activity to regulate the neuronal response to sound from different locations in space and suggest that the tegmental thalamo-cortical pathway is normally suppressed in young animals. Population rate and latency codes of acoustic space were also impaired by normal aging, which resulted in an age-related change in the population's representation of acoustic space in azimuth (see Figure 3). This lack of inhibition is likely also responsible for the non-monotonic response as a function of time in the aged animals, particularly at nearby but non-best directions, as a function of time (see Figure 2). These results suggest that one of the main central effects of normal aging is the perturbation of the timing and efficacy of inhibition of auditory cortical responses.

Bottom Line: It is also possible that spatial tuning was decreased as a consequence of reduced inhibition at non-best locations.In this report we found that aged animals had greater activity throughout the response period, but primarily during the onset of the response.These results can be interpreted in the context of a failure of the timing and efficiency of feed-forward thalamo-cortical and cortico-cortical circuits in aged animals.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology and Center for Neuroscience, University of California at Davis Davis, CA, USA ; Evelyn F. McKnight Brain Institute and ARL Division of Neural Systems, Memory and Aging, University of Arizona Tucson, AZ, USA.

ABSTRACT
Age-related hearing deficits are a leading cause of disability among the aged. While some forms of hearing deficits are peripheral in origin, others are centrally mediated. One such deficit is the ability to localize sounds, a critical component for segregating different acoustic objects and events, which is dependent on the auditory cortex. Recent evidence indicates that in aged animals the normal sharpening of spatial tuning between neurons in primary auditory cortex to the caudal lateral field does not occur as it does in younger animals. As a decrease in inhibition with aging is common in the ascending auditory system, it is possible that this lack of spatial tuning sharpening is due to a decrease in inhibition at different periods within the response. It is also possible that spatial tuning was decreased as a consequence of reduced inhibition at non-best locations. In this report we found that aged animals had greater activity throughout the response period, but primarily during the onset of the response. This was most prominent at non-best directions, which is consistent with the hypothesis that inhibition is a primary mechanism for sharpening spatial tuning curves. We also noted that in aged animals the latency of the response was much shorter than in younger animals, which is consistent with a decrease in pre-onset inhibition. These results can be interpreted in the context of a failure of the timing and efficiency of feed-forward thalamo-cortical and cortico-cortical circuits in aged animals. Such a mechanism, if generalized across cortical areas, could play a major role in age-related cognitive decline.

No MeSH data available.


Related in: MedlinePlus