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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

Population inhibitory tuning index comparison between young and aged animals. The inhibitory index showed a significant difference between young and aged A1 neurons during the early and off response periods (Panel A). Panel (B) shows that the strength of inhibition or suppressed response is greater in young animals compared to aged animals for CL neurons (*p < 0.05; **p < 0.01; ***p < 0.001).
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Figure 6: Population inhibitory tuning index comparison between young and aged animals. The inhibitory index showed a significant difference between young and aged A1 neurons during the early and off response periods (Panel A). Panel (B) shows that the strength of inhibition or suppressed response is greater in young animals compared to aged animals for CL neurons (*p < 0.05; **p < 0.01; ***p < 0.001).

Mentions: In order to investigate the inhibitory processes across spatial locations in neurons from aged and young animals, we first examined how much relative inhibitory activity was present across the population of neurons in the worst direction during the three different response periods. We used the rate-based ITI to quantify the strength of a suppressed response, defined as a response that was less than the spontaneous rate. ITI values range from −1 for strongly suppressed responses to 1 for strongly excitatory responses. ITI values greater than and equal to 0 indicate that the response in the worst direction was equal to the spontaneous rate (see Methods). The results of this analysis are shown in Figure 6. In A1 neurons of young monkeys, the strength of inhibition or suppressed responses continuously increased (Tukey Test, p < 0.001) over the early, late, and off response periods, F(2, 1275) = 259.34, p < 0.001. In CL neurons of young monkeys, the increase in strength of inhibition or suppressed responses was restricted, however, to the early and late period (Tukey Test, p < 0.001) of the response, F(2, 1275) = 119.94, p < 0.001. This finding is consistent with our data presented in Figures 2 and 3, which shows a response decrement over the response period. In the second layer of this analysis, we examined the strength of inhibition during the early, late, and off response periods between A1 and CL to determine if greater inhibition or response suppression contributes to changes along the cortical hierarchy. In young monkeys, we found that the strength of inhibition was consistently stronger on CL neurons than on A1 neurons across the early [F(1, 1276) = 71.66, p < 0.001], late [F(1, 1276) = 126.96, p < 0.001], and off [F(1, 1276) = 9.10, p < 0.01] response periods. This indicates a greater inhibition or response suppression in the worst direction along the cortical hierarchy. In the next layer of the analysis, we examined if the strength of inhibition decreased during the early, late, and off response periods as a function of age for neurons in A1 (Figure 6A) and CL (Figure 6B). We found an age-related decrease for A1 neurons (Figure 6A), where aged neurons in A1 were less suppressed during the early [F(1, 1276) = 25.95, p < 0.001] and off [F(1, 1276) = 23.31, p < 0.001] periods. We also found an age-related decrease in the strength of inhibition on suppressed responses in CL neurons (Figure 6B), where aged neurons in CL were consistently less suppressed during the early [F(1, 1276) = 4.62, p < 0.05], late [F(1, 1276) = 13.22, p < 0.001] and off [F(1, 1276) = 9.24, p < 0.01] periods. This suggests that there is an age-related imbalance of inhibitory and excitatory activity on the regulation of the neural response in the worst direction.


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)

Population inhibitory tuning index comparison between young and aged animals. The inhibitory index showed a significant difference between young and aged A1 neurons during the early and off response periods (Panel A). Panel (B) shows that the strength of inhibition or suppressed response is greater in young animals compared to aged animals for CL neurons (*p < 0.05; **p < 0.01; ***p < 0.001).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Population inhibitory tuning index comparison between young and aged animals. The inhibitory index showed a significant difference between young and aged A1 neurons during the early and off response periods (Panel A). Panel (B) shows that the strength of inhibition or suppressed response is greater in young animals compared to aged animals for CL neurons (*p < 0.05; **p < 0.01; ***p < 0.001).
Mentions: In order to investigate the inhibitory processes across spatial locations in neurons from aged and young animals, we first examined how much relative inhibitory activity was present across the population of neurons in the worst direction during the three different response periods. We used the rate-based ITI to quantify the strength of a suppressed response, defined as a response that was less than the spontaneous rate. ITI values range from −1 for strongly suppressed responses to 1 for strongly excitatory responses. ITI values greater than and equal to 0 indicate that the response in the worst direction was equal to the spontaneous rate (see Methods). The results of this analysis are shown in Figure 6. In A1 neurons of young monkeys, the strength of inhibition or suppressed responses continuously increased (Tukey Test, p < 0.001) over the early, late, and off response periods, F(2, 1275) = 259.34, p < 0.001. In CL neurons of young monkeys, the increase in strength of inhibition or suppressed responses was restricted, however, to the early and late period (Tukey Test, p < 0.001) of the response, F(2, 1275) = 119.94, p < 0.001. This finding is consistent with our data presented in Figures 2 and 3, which shows a response decrement over the response period. In the second layer of this analysis, we examined the strength of inhibition during the early, late, and off response periods between A1 and CL to determine if greater inhibition or response suppression contributes to changes along the cortical hierarchy. In young monkeys, we found that the strength of inhibition was consistently stronger on CL neurons than on A1 neurons across the early [F(1, 1276) = 71.66, p < 0.001], late [F(1, 1276) = 126.96, p < 0.001], and off [F(1, 1276) = 9.10, p < 0.01] response periods. This indicates a greater inhibition or response suppression in the worst direction along the cortical hierarchy. In the next layer of the analysis, we examined if the strength of inhibition decreased during the early, late, and off response periods as a function of age for neurons in A1 (Figure 6A) and CL (Figure 6B). We found an age-related decrease for A1 neurons (Figure 6A), where aged neurons in A1 were less suppressed during the early [F(1, 1276) = 25.95, p < 0.001] and off [F(1, 1276) = 23.31, p < 0.001] periods. We also found an age-related decrease in the strength of inhibition on suppressed responses in CL neurons (Figure 6B), where aged neurons in CL were consistently less suppressed during the early [F(1, 1276) = 4.62, p < 0.05], late [F(1, 1276) = 13.22, p < 0.001] and off [F(1, 1276) = 9.24, p < 0.01] periods. This suggests that there is an age-related imbalance of inhibitory and excitatory activity on the regulation of the neural response in the worst direction.

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