Abstract
Most mammals possess high-resolution visual perception, with primary visual cortices containing fine-scale, inter-related feature representations (for example, orientation and ocular dominance). Rats lack precise vision, but their vibrissa sensory system provides a precise tactile modality, including vibrissa-related 'barrel' columns in primary somatosensory cortex. Here, we examined the subcolumnar organization of direction preference and somatotopy using a new omni-directional, multi-vibrissa stimulator. We discovered a direction map that was systematically linked to somatotopy, such that neurons were tuned for motion toward their preferred surround vibrissa. This sub-barrel column direction map demonstrated an emergent refinement from layer IV to layer II/III. These data suggest that joint processing of multiple sensory features is a common property of high-resolution sensory systems.
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Acknowledgements
We thank J. Ritt, A. Nelson, M. Sur, C. Reid, R. Desimone and R. Born for feedback, and K. Kempadoo and A. Ramanathan for histology. We thank the US National Institutes of Health, the National Science Foundation, the McGovern Institute for Brain Research (C.I.M.) and the Howard Hughes Medical Institute (M.L.A.) for supporting this work.
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Supplementary Fig. 1
Methodological Approaches A. Left: A photograph of the stimulator employed. Movements were driven by piezoelectric elements poled for operation in 2 axes: Combinations of these axes through a pair of driving signals and piezoelectric amplifiers dedicated to each stimulator allowed omni-directional control. The label 'a' denotes the piezoelectric element, and 'b' the custom capillary vibrissa holder. B. A cartoon of the 4-tetrode arrays showing the aspect ratio of the electrodes. C. A reconstruction of a D3 barrel showing two reconstructed electrode positions from a single penetration of the array. The bounding square and bisecting lines show the parameters recorded for reconstruction and alignment of barrels across experiments. D. A bar plot showing the fall-off in peak action potential amplitude across contacts on a tetrode. When a significant trigger was recorded, the contact with the largest amplitude spike was identified, and the peak amplitude of the spike signal within .5msec on the other contacts calculated. Data shown were taken from single-units (N = 420) to ensure accurate isolation. Spike amplitudes reduced to 53% at an inter-contact distance of 35m and 41% at 50m. Because of the stringent cut-off applied for acceptance spikes (5 standard deviations above background), these findings suggest that most neurons were located less than ˜50m from the most proximal contact. (PDF 659 kb)
Supplementary Fig. 2
Correlation Between Somatotopy and Anatomic Position within a Barrel Column The relation between the anatomic barrel position and somatotopic center of mass are plotted for the anterior-posterior axis (top) and inferior-superior axis (bottom). Symbols/colors indicate individual experiments. A significant correlation was observed between somatotopy and anatomic position along the anterior-posterior axis in layers IV (r = .44, p < .0001, N = 71) and II/III (r = .34, p = .004, N = 58). A significant correlation was also observed between somatotopy and anatomic position along the inferior-superior axis in layers IV (r = .34, p = .002, N = 71) and II/III (r = .56, p = .0001, N = 58). Note, however, that the range of somatotopic values along the inferior-superior axis is considerably truncated. (PDF 235 kb)
Supplementary Fig. 3
Direction Preference Analysis for Multi-Unit Maps of Layers IV and II/III Left Somatotopic direction maps, angular prediction calculations and quartile distributions of tuning values for multi-unit activity (MUA: See Figures 2, 4 and 5 in paper and accompany text). Data were culled from 111 recording sites in layer II/III and 112 in layer IV (N/quartile = 28 for both). The non-rotated map revealed a significant difference in direction preferences between 1st and 4th quartiles in layer II/III (p = .0024, difference in mean rostral-caudal preference = .41) and a marginal association in layer IV (p = .09, .23). After rotation to the optimal axis (see text), these differences increased and were significant in both laminae (layer II/III: -500 rotation, p < .0001, .68; layer IV: -430 rotation, p = .009, .37). (PDF 311 kb)
Supplementary Fig. 4
Scatter Plots Showing the Association of Direction Preference Across Laminae Plots are shown for the 3 cell groupings analyzed, All neurons (including those unclassified: N = 149), RSUs (N = 36) and FSUs (N = 31). For all plots, the unity line and lines bounding a 450 window of similarity are shown. Red dots indicate neuron pairs that showed < +450 difference in tuning. As shown in Figure 6A, RSUs revealed a significant sub-population (18/36 pairs; 50% of the sample; chance = 25%) that demonstrated less than or equal to a 450 difference in tuning across layers. This trend was present but weaker in the All neurons grouping and absent in the FSUs. Angular-angular correlations were weak but significant for RSUs (r = .06, p < .001) and All neurons (r = .001, p < .001) but were not significant for FSUs (r = .0007, p > .05) (PDF 135 kb)
Supplementary Fig. 5
Shifts in Direction Preference Across Laminae for RSUs and FSUs Maps are shown of shifts in direction preference for RSUs and FSUs for non-columnar cell pairs (left) and columnar (right) (see Figure 6 in paper and text). Scatter plots are also shown relating shift in direction preference to the layer II/III somatotopic position. As with analysis of All neurons (Figure 6C), these sub-populations showed a systematic pattern of shifts for non-columnar cell pairs, with anterior somatotopic tuning positions shifting rostral, and posterior somatotopic recordings shifting caudal. Linear regressions fit to non-columnar positions (black line and points) and columnar positions (gray line and points) showed a significant correlation for non-columnar sites (RSUs: r = .65, p = .002, N = 18; FSUs: r = .52, p = .007, N = 22) but not for columnar sites (RSUs: r = -.09, p = .35, N = 18; FSUs: r = -.17, p = .33, N = 9). (PDF 137 kb)
Supplementary Fig. 6
An Idealized Model of Direction Representation in Layers IV and II/III The data presented support the model shown, in which an outwardly radiating direction preference map is observed in the supragranular layers that is dominated by rostral and caudal direction preferences. This map emerges from a more disorganized preference distribution within layer IV. Across layers, those RSUs that demonstrated a correlation between direction preference and somatotopy showed columnar organization. Arrows and red and blue colors indicate the rostral or caudal direction preference of a given spatial position. Dashed gray arrows indicate the prediction that direction maps in surrounding barrel columns will demonstrate contrasting direction tuning at the somatotopic border between the two vibrissa representations. (PDF 299 kb)
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Andermann, M., Moore, C. A somatotopic map of vibrissa motion direction within a barrel column. Nat Neurosci 9, 543–551 (2006). https://doi.org/10.1038/nn1671
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DOI: https://doi.org/10.1038/nn1671
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