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Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation

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ABSTRACT

Sensory cortices do not work in isolation. The functional responses of neurons in primary sensory cortices can be affected by activity from other modalities. For example, short-term visual deprivations, or dark exposure (DE), leads to enhanced neuronal responses and frequency selectivity to sounds in layer 4 (L4) of primary auditory cortex (A1). Circuit changes within A1 likely underlie these changes. Prior studies revealed that DE enhanced thalamocortical transmission to L4 in A1. Because the frequency selectivity of L4 neurons is determined by both thalamocortical and intracortical inputs, changes in intralaminar circuits to L4 neurons might also contribute to improved sound responses. We thus investigated in mouse A1 whether intracortical circuits to L4 cells changed after DE. Using in vitro whole-cell patch recordings in thalamocortical slices from mouse auditory cortex, we show that DE can lead to refinement of interlaminar excitatory as well as inhibitory connections from L2/3 to L4 cells, manifested as a weakening of these connections. The circuit refinement is present along the tonotopic axis, indicating reduced integration along the tonotopic axis. Thus, cross-modal influences may alter the spectral and temporal processing of sensory stimuli in multiple cortical layers by refinement of thalamocortical and intracortical circuits.

No MeSH data available.


The balance of excitation and inhibition of L2/3 inputs to L4 is reduced. Cumulative distributions (CDFs) of excitation/inhibition (EI) area ratio (left), charge ratio (middle), and peak amplitude ratio (right) from L2/3 (top), L4 (middle), and L5/6 (bottom) in NR and DE cells. The charge ratio of L2/3 inputs decreased after DE (EI area ratio: L2/3: p = 0.2, L4: p = 0.53, L5/6: p = 0.55; EI charge ratio: L2/3: p = 0.007, L4: p = 0.26, L5/6: p = 0.08; EI amplitude ratio: L2/3: p = 0.12, L4: p = 0.29, L5/6: p = 0.90). All comparisons were done with Wilcoxon rank-sum test or Student’s t test.
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Figure 6: The balance of excitation and inhibition of L2/3 inputs to L4 is reduced. Cumulative distributions (CDFs) of excitation/inhibition (EI) area ratio (left), charge ratio (middle), and peak amplitude ratio (right) from L2/3 (top), L4 (middle), and L5/6 (bottom) in NR and DE cells. The charge ratio of L2/3 inputs decreased after DE (EI area ratio: L2/3: p = 0.2, L4: p = 0.53, L5/6: p = 0.55; EI charge ratio: L2/3: p = 0.007, L4: p = 0.26, L5/6: p = 0.08; EI amplitude ratio: L2/3: p = 0.12, L4: p = 0.29, L5/6: p = 0.90). All comparisons were done with Wilcoxon rank-sum test or Student’s t test.

Mentions: DE results in a balanced refinement of excitatory and inhibitory connections to L2/3 neurons (Meng et al., 2015). Because thalamic input to L4 neurons is increased after DE (Petrus et al., 2014), the adjustment of intracortical circuits to L4 neurons might compensate for this additional driving input. We thus investigated whether the changes in the spatial pattern of excitatory and inhibitory connection to L4 neurons occur in a balanced manner. We computed the excitation/inhibition (EI) ratio based on input area, transferred charge, and peak amplitude for every cell. Because we could not assess excitatory input in locations that gave direct responses for excitation, we excluded those stimulus locations in our calculations for both excitation and inhibition. Our calculations showed that the EI ratio for L2/3 inputs decreased after DE (Fig. 6), indicating that L4 neurons received less excitatory input from L2/3. This suggests that increased firing rates in response to sound stimulation after DE are due to increased thalamocortical input (Petrus et al., 2014).


Intracortical Circuits in Thalamorecipient Layers of Auditory Cortex Refine after Visual Deprivation
The balance of excitation and inhibition of L2/3 inputs to L4 is reduced. Cumulative distributions (CDFs) of excitation/inhibition (EI) area ratio (left), charge ratio (middle), and peak amplitude ratio (right) from L2/3 (top), L4 (middle), and L5/6 (bottom) in NR and DE cells. The charge ratio of L2/3 inputs decreased after DE (EI area ratio: L2/3: p = 0.2, L4: p = 0.53, L5/6: p = 0.55; EI charge ratio: L2/3: p = 0.007, L4: p = 0.26, L5/6: p = 0.08; EI amplitude ratio: L2/3: p = 0.12, L4: p = 0.29, L5/6: p = 0.90). All comparisons were done with Wilcoxon rank-sum test or Student’s t test.
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Figure 6: The balance of excitation and inhibition of L2/3 inputs to L4 is reduced. Cumulative distributions (CDFs) of excitation/inhibition (EI) area ratio (left), charge ratio (middle), and peak amplitude ratio (right) from L2/3 (top), L4 (middle), and L5/6 (bottom) in NR and DE cells. The charge ratio of L2/3 inputs decreased after DE (EI area ratio: L2/3: p = 0.2, L4: p = 0.53, L5/6: p = 0.55; EI charge ratio: L2/3: p = 0.007, L4: p = 0.26, L5/6: p = 0.08; EI amplitude ratio: L2/3: p = 0.12, L4: p = 0.29, L5/6: p = 0.90). All comparisons were done with Wilcoxon rank-sum test or Student’s t test.
Mentions: DE results in a balanced refinement of excitatory and inhibitory connections to L2/3 neurons (Meng et al., 2015). Because thalamic input to L4 neurons is increased after DE (Petrus et al., 2014), the adjustment of intracortical circuits to L4 neurons might compensate for this additional driving input. We thus investigated whether the changes in the spatial pattern of excitatory and inhibitory connection to L4 neurons occur in a balanced manner. We computed the excitation/inhibition (EI) ratio based on input area, transferred charge, and peak amplitude for every cell. Because we could not assess excitatory input in locations that gave direct responses for excitation, we excluded those stimulus locations in our calculations for both excitation and inhibition. Our calculations showed that the EI ratio for L2/3 inputs decreased after DE (Fig. 6), indicating that L4 neurons received less excitatory input from L2/3. This suggests that increased firing rates in response to sound stimulation after DE are due to increased thalamocortical input (Petrus et al., 2014).

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Sensory cortices do not work in isolation. The functional responses of neurons in primary sensory cortices can be affected by activity from other modalities. For example, short-term visual deprivations, or dark exposure (DE), leads to enhanced neuronal responses and frequency selectivity to sounds in layer 4 (L4) of primary auditory cortex (A1). Circuit changes within A1 likely underlie these changes. Prior studies revealed that DE enhanced thalamocortical transmission to L4 in A1. Because the frequency selectivity of L4 neurons is determined by both thalamocortical and intracortical inputs, changes in intralaminar circuits to L4 neurons might also contribute to improved sound responses. We thus investigated in mouse A1 whether intracortical circuits to L4 cells changed after DE. Using in vitro whole-cell patch recordings in thalamocortical slices from mouse auditory cortex, we show that DE can lead to refinement of interlaminar excitatory as well as inhibitory connections from L2/3 to L4 cells, manifested as a weakening of these connections. The circuit refinement is present along the tonotopic axis, indicating reduced integration along the tonotopic axis. Thus, cross-modal influences may alter the spectral and temporal processing of sensory stimuli in multiple cortical layers by refinement of thalamocortical and intracortical circuits.

No MeSH data available.