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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

Pre-onset inhibition in young but not aged monkeys. Each panel shows the bins that have significantly less (blue) or significantly more (red) activity compared to spontaneous. The population response of young animals is shown at the left, aged animals to the right, with A1 neurons in the top row and CL neurons in the bottom row. A1 of young animals shows pre-onset inhibition at the directions farthest from the best direction, but in CL this is true across a broader spatial extent (bottom left). In contrast, aged animals show no pre-onset inhibition at any direction.
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Figure 9: Pre-onset inhibition in young but not aged monkeys. Each panel shows the bins that have significantly less (blue) or significantly more (red) activity compared to spontaneous. The population response of young animals is shown at the left, aged animals to the right, with A1 neurons in the top row and CL neurons in the bottom row. A1 of young animals shows pre-onset inhibition at the directions farthest from the best direction, but in CL this is true across a broader spatial extent (bottom left). In contrast, aged animals show no pre-onset inhibition at any direction.

Mentions: Inspecting the population first-spike tuning curves in young monkeys revealed that the fastest excitatory response was much faster (~8 ms) in CL than what was measured in A1. This was particularly noted in the population responses shown in Figures 2 and 3 when the axis is rotated to illustrate age-differences vertically. This result, along with the temporal tuning results, suggests that the population response in CL may be primed and refined by an initial coordinated volley of inhibitory activity by the tegmental pathway. To test this hypothesis, we re-examined the pre-onset response for significant inhibitory bins in A1 and CL. Figure 9 illustrates significant excitatory and inhibitory bins during the first 50 ms of the population response as a function of the spatial distance from the best direction. Significant excitatory bins are colored in red, significant inhibitory bins are colored in blue, and bins that were not significantly different from spontaneous activity are colored in green. In young monkeys (left column), we found that area CL had significantly more inhibitory bins than area A1 (χ2, p < 0.05). In A1, we found 14 significant inhibitory bins that flanked the best direction prior to response onset (Figure 9 top left). In CL there was much more inhibitory activity at the flanking locations (Figure 9 bottom left). These results suggest that CL normally receives both a volley of excitation in the best direction and a volley of inhibitory activity that flanks the best direction that arrives simultaneously or slightly preceding the volley of activity into area A1. This implies that a function of the parallel thalamo-cortical pathway into area CL is involved in shaping and refining spatial tuning curves. Interestingly, we did not find a single inhibitory bin prior to the response onset in area A1 or CL of aged monkeys (Figure 9 right column). This indicates that the mechanism of inhibiting the non-best directions is abolished in aged animals, which could account for some, if not all, of the differences in spatial tuning seen in CL between young and aged animals.


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)

Pre-onset inhibition in young but not aged monkeys. Each panel shows the bins that have significantly less (blue) or significantly more (red) activity compared to spontaneous. The population response of young animals is shown at the left, aged animals to the right, with A1 neurons in the top row and CL neurons in the bottom row. A1 of young animals shows pre-onset inhibition at the directions farthest from the best direction, but in CL this is true across a broader spatial extent (bottom left). In contrast, aged animals show no pre-onset inhibition at any direction.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 9: Pre-onset inhibition in young but not aged monkeys. Each panel shows the bins that have significantly less (blue) or significantly more (red) activity compared to spontaneous. The population response of young animals is shown at the left, aged animals to the right, with A1 neurons in the top row and CL neurons in the bottom row. A1 of young animals shows pre-onset inhibition at the directions farthest from the best direction, but in CL this is true across a broader spatial extent (bottom left). In contrast, aged animals show no pre-onset inhibition at any direction.
Mentions: Inspecting the population first-spike tuning curves in young monkeys revealed that the fastest excitatory response was much faster (~8 ms) in CL than what was measured in A1. This was particularly noted in the population responses shown in Figures 2 and 3 when the axis is rotated to illustrate age-differences vertically. This result, along with the temporal tuning results, suggests that the population response in CL may be primed and refined by an initial coordinated volley of inhibitory activity by the tegmental pathway. To test this hypothesis, we re-examined the pre-onset response for significant inhibitory bins in A1 and CL. Figure 9 illustrates significant excitatory and inhibitory bins during the first 50 ms of the population response as a function of the spatial distance from the best direction. Significant excitatory bins are colored in red, significant inhibitory bins are colored in blue, and bins that were not significantly different from spontaneous activity are colored in green. In young monkeys (left column), we found that area CL had significantly more inhibitory bins than area A1 (χ2, p < 0.05). In A1, we found 14 significant inhibitory bins that flanked the best direction prior to response onset (Figure 9 top left). In CL there was much more inhibitory activity at the flanking locations (Figure 9 bottom left). These results suggest that CL normally receives both a volley of excitation in the best direction and a volley of inhibitory activity that flanks the best direction that arrives simultaneously or slightly preceding the volley of activity into area A1. This implies that a function of the parallel thalamo-cortical pathway into area CL is involved in shaping and refining spatial tuning curves. Interestingly, we did not find a single inhibitory bin prior to the response onset in area A1 or CL of aged monkeys (Figure 9 right column). This indicates that the mechanism of inhibiting the non-best directions is abolished in aged animals, which could account for some, if not all, of the differences in spatial tuning seen in CL between young and aged animals.

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