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The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits.

Oviedo HV, Bureau I, Svoboda K, Zador AM - Nat. Neurosci. (2010)

Bottom Line: By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column.In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3.Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

ABSTRACT
The primary auditory cortex (A1) is organized tonotopically, with neurons sensitive to high and low frequencies arranged in a rostro-caudal gradient. We used laser scanning photostimulation in acute slices to study the organization of local excitatory connections onto layers 2 and 3 (L2/3) of the mouse A1. Consistent with the organization of other cortical regions, synaptic inputs along the isofrequency axis (orthogonal to the tonotopic axis) arose predominantly within a column. By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column. In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3. Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

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Synaptic input organization along the tonotopic axis(a) Horizontal slices used to capture the anterior-posterior (A↔P) representation of tonotopy in auditory cortex. Image of a horizontal slice depicting the anatomical landmarks used to align the stimulation grid (white box). The anterior (left) side of the slice corresponds to the putative high frequency (Hi F) portion of A1 and the posterior (right) side to putative low frequencies (Low F). (b) Trace map of synaptic input map to a L2 neuron (top) and its colormap (middle). Interpolated population map of all L2 neurons recorded (bottom, n = 15). (c) Single-cell trace map (top) and colormap (middle), and interpolated population map (bottom) of all L3 neurons recorded (n = 15). (d) Summary of the mean laminar input to L2 and L3 arising from all cortical layers. Asterisk indicates laminar input where the difference in synaptic input between L2 and L3 was significantly different (P < 0.05, n = 30, t-test). (e) Grand summary and comparison of the mean laminar input to L2/3 along the isofrequency (IF) and tonotopic (TT) axes. Asterisk indicates laminar input where the difference in synaptic input between the tonotopic and isofrequency axes was significantly different (P << 0.01, t-test). Data are presented as mean ± s.e.m. Scale bars in synaptic traces are 50 pA and 100 ms.
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Figure 3: Synaptic input organization along the tonotopic axis(a) Horizontal slices used to capture the anterior-posterior (A↔P) representation of tonotopy in auditory cortex. Image of a horizontal slice depicting the anatomical landmarks used to align the stimulation grid (white box). The anterior (left) side of the slice corresponds to the putative high frequency (Hi F) portion of A1 and the posterior (right) side to putative low frequencies (Low F). (b) Trace map of synaptic input map to a L2 neuron (top) and its colormap (middle). Interpolated population map of all L2 neurons recorded (bottom, n = 15). (c) Single-cell trace map (top) and colormap (middle), and interpolated population map (bottom) of all L3 neurons recorded (n = 15). (d) Summary of the mean laminar input to L2 and L3 arising from all cortical layers. Asterisk indicates laminar input where the difference in synaptic input between L2 and L3 was significantly different (P < 0.05, n = 30, t-test). (e) Grand summary and comparison of the mean laminar input to L2/3 along the isofrequency (IF) and tonotopic (TT) axes. Asterisk indicates laminar input where the difference in synaptic input between the tonotopic and isofrequency axes was significantly different (P << 0.01, t-test). Data are presented as mean ± s.e.m. Scale bars in synaptic traces are 50 pA and 100 ms.

Mentions: To examine specific differences between inputs to L2 and L3 we examined the average input to each layer separately (Fig. 2d, right). Neurons in L2 and L3 were readily distinguished based on previously described laminar boundaries 11, and our own experimental observations that: (1) L2 appears as the densest cortical layer under infrared gradient contrast optics (average thickness of 100 µm; see Fig. 3a); and (2) there are significant morphological differences between neurons in L2 and L3 (see Fig. 6a–b for examples and ref. 6). Layer 2 neurons had a non-classic pyramidal shape with their apical dendrites branching close to the cell body, whereas L3 neurons had a classic pyramidal shape. Quantitative comparison of the inputs to L2 (n = 11 neurons) and L3 (n = 15 neurons) revealed largely similar inputs into both layers, with the exception of significant input from deep layers into L2 but not L3 (Fig. 2d, right). This input arose from the border of L5/6 and was not observed in the rat auditory cortex8. Layer 3 had strong recurrent connections that are also largely absent in the rat. However, given the extensive lemniscal thalamocortical projections in L3 of the mouse 12, the prominent L3 to L3 connections we observe in the mouse may not represent a significant deviation from the classic L4 to L3 pathway.


The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits.

Oviedo HV, Bureau I, Svoboda K, Zador AM - Nat. Neurosci. (2010)

Synaptic input organization along the tonotopic axis(a) Horizontal slices used to capture the anterior-posterior (A↔P) representation of tonotopy in auditory cortex. Image of a horizontal slice depicting the anatomical landmarks used to align the stimulation grid (white box). The anterior (left) side of the slice corresponds to the putative high frequency (Hi F) portion of A1 and the posterior (right) side to putative low frequencies (Low F). (b) Trace map of synaptic input map to a L2 neuron (top) and its colormap (middle). Interpolated population map of all L2 neurons recorded (bottom, n = 15). (c) Single-cell trace map (top) and colormap (middle), and interpolated population map (bottom) of all L3 neurons recorded (n = 15). (d) Summary of the mean laminar input to L2 and L3 arising from all cortical layers. Asterisk indicates laminar input where the difference in synaptic input between L2 and L3 was significantly different (P < 0.05, n = 30, t-test). (e) Grand summary and comparison of the mean laminar input to L2/3 along the isofrequency (IF) and tonotopic (TT) axes. Asterisk indicates laminar input where the difference in synaptic input between the tonotopic and isofrequency axes was significantly different (P << 0.01, t-test). Data are presented as mean ± s.e.m. Scale bars in synaptic traces are 50 pA and 100 ms.
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Figure 3: Synaptic input organization along the tonotopic axis(a) Horizontal slices used to capture the anterior-posterior (A↔P) representation of tonotopy in auditory cortex. Image of a horizontal slice depicting the anatomical landmarks used to align the stimulation grid (white box). The anterior (left) side of the slice corresponds to the putative high frequency (Hi F) portion of A1 and the posterior (right) side to putative low frequencies (Low F). (b) Trace map of synaptic input map to a L2 neuron (top) and its colormap (middle). Interpolated population map of all L2 neurons recorded (bottom, n = 15). (c) Single-cell trace map (top) and colormap (middle), and interpolated population map (bottom) of all L3 neurons recorded (n = 15). (d) Summary of the mean laminar input to L2 and L3 arising from all cortical layers. Asterisk indicates laminar input where the difference in synaptic input between L2 and L3 was significantly different (P < 0.05, n = 30, t-test). (e) Grand summary and comparison of the mean laminar input to L2/3 along the isofrequency (IF) and tonotopic (TT) axes. Asterisk indicates laminar input where the difference in synaptic input between the tonotopic and isofrequency axes was significantly different (P << 0.01, t-test). Data are presented as mean ± s.e.m. Scale bars in synaptic traces are 50 pA and 100 ms.
Mentions: To examine specific differences between inputs to L2 and L3 we examined the average input to each layer separately (Fig. 2d, right). Neurons in L2 and L3 were readily distinguished based on previously described laminar boundaries 11, and our own experimental observations that: (1) L2 appears as the densest cortical layer under infrared gradient contrast optics (average thickness of 100 µm; see Fig. 3a); and (2) there are significant morphological differences between neurons in L2 and L3 (see Fig. 6a–b for examples and ref. 6). Layer 2 neurons had a non-classic pyramidal shape with their apical dendrites branching close to the cell body, whereas L3 neurons had a classic pyramidal shape. Quantitative comparison of the inputs to L2 (n = 11 neurons) and L3 (n = 15 neurons) revealed largely similar inputs into both layers, with the exception of significant input from deep layers into L2 but not L3 (Fig. 2d, right). This input arose from the border of L5/6 and was not observed in the rat auditory cortex8. Layer 3 had strong recurrent connections that are also largely absent in the rat. However, given the extensive lemniscal thalamocortical projections in L3 of the mouse 12, the prominent L3 to L3 connections we observe in the mouse may not represent a significant deviation from the classic L4 to L3 pathway.

Bottom Line: By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column.In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3.Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

ABSTRACT
The primary auditory cortex (A1) is organized tonotopically, with neurons sensitive to high and low frequencies arranged in a rostro-caudal gradient. We used laser scanning photostimulation in acute slices to study the organization of local excitatory connections onto layers 2 and 3 (L2/3) of the mouse A1. Consistent with the organization of other cortical regions, synaptic inputs along the isofrequency axis (orthogonal to the tonotopic axis) arose predominantly within a column. By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column. In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3. Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

Show MeSH