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A radial map of multi-whisker correlation selectivity in the rat barrel cortex

View Article: PubMed Central - PubMed

ABSTRACT

In the barrel cortex, several features of single-whisker stimuli are organized in functional maps. The barrel cortex also encodes spatio-temporal correlation patterns of multi-whisker inputs, but so far the cortical mapping of neurons tuned to such input statistics is unknown. Here we report that layer 2/3 of the rat barrel cortex contains an additional functional map based on neuronal tuning to correlated versus uncorrelated multi-whisker stimuli: neuron responses to uncorrelated multi-whisker stimulation are strongest above barrel centres, whereas neuron responses to correlated and anti-correlated multi-whisker stimulation peak above the barrel–septal borders, forming rings of multi-whisker synchrony-preferring cells.

No MeSH data available.


A model of multi-whisker supra-linear integration in barrel cortex layer 2/3.(a) Radial distribution of mean dF/F response to the PW (green) and to the sum of the two closest adjacent whiskers (black). ***Mann-Whitney P=8.1 × 10−4 for PW and *P=0.024 for adjacent whiskers. (b) A simple model of the projections to the barrel and septal compartments. A supra-linear integration of VPm-head and VPm-core inputs during correlated stimulation may occur in neurons above the barrel-septa border that receive both inputs, while neurons above barrel centre and septum centre mainly receive a single source of input and are therefore not subjected to the same mechanism. Bar., barrel.
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f5: A model of multi-whisker supra-linear integration in barrel cortex layer 2/3.(a) Radial distribution of mean dF/F response to the PW (green) and to the sum of the two closest adjacent whiskers (black). ***Mann-Whitney P=8.1 × 10−4 for PW and *P=0.024 for adjacent whiskers. (b) A simple model of the projections to the barrel and septal compartments. A supra-linear integration of VPm-head and VPm-core inputs during correlated stimulation may occur in neurons above the barrel-septa border that receive both inputs, while neurons above barrel centre and septum centre mainly receive a single source of input and are therefore not subjected to the same mechanism. Bar., barrel.

Mentions: Our study provides evidences for the existence of two maps, for correlated and anti-correlated stimulation-preferring neurons, both with a ring shape above the barrel–septum border. We showed that they spatially correspond to locations where supra-linearity properties dominate, allowing the boost of cell responses to synchronous multi-whisker activation. Why would the supra-linearity be located above the barrel–septum border, building a correlation map that largely escapes the area above barrel? It may arise from integration at multiple stages of the thalamo-cortical loop10 as well as from local cortical processing. On the basis of our observations, we propose a cortical model of supra-linear integration of multi-whisker inputs. Thalamic inputs to layer 2/3 neurons have three main origins: (i) mono-whisker inputs come from VPm-core in layer 4 barrels, and are then vertically relayed to layers 2/3. (ii) Multi-whisker inputs are conveyed by VPm-head11 to layer 4 septa, and then again vertically relayed to layers 2/3 (ref. 12). (iii) Multi-whisker inputs can also originate in POm and reach layer 1, where it connects to layer 2/3 dendritic arbors. However, recent studies have shown that in anaesthetized animals sensory transmission through this nucleus is often strongly diminished or impeded by feed-forward inhibition from the zona incerta1314. Because of their uneven distribution above barrel and septa, the pathways (i) and (ii) could contribute to the emergence of the map. The spatial profile of the response to deflections of the PW is centred on the corresponding barrel, due to VPm-core inputs. VPm-head inputs centre the response to surrounding whiskers above the septa, as observed in Fig. 5a, where the radial distribution of the responses to PW and to the sum of two closest adjacent whiskers is plotted. Depending on their location, neurons in layer 2/3 could thus have three patterns of input (Fig. 5b): mainly mono-whisker (PW) inputs above barrels; mainly multi-whisker inputs above septa; and a combination of both above the border between barrel and septa. In the case of layer 2/3 neurons above the barrel–septa border, supra-linear summation of PW and surround inputs during correlated or anti-correlated stimulations could then occur, through nonlinear dendritic integration1516. Figure 5b illustrates the expected profile of the supra-linearity. This model predicts a map for correlation-preferring neurons with a ring shape aligned vertically with each barrel border, differing from the simple two-component (barrel and septa) domains, and the existence of a nonlinear cortical integration in the multi-whisker processing that should appear to be non-uniform above barrel and septa. The same mechanism could account for the map for anti-correlation-preferring neurons.


A radial map of multi-whisker correlation selectivity in the rat barrel cortex
A model of multi-whisker supra-linear integration in barrel cortex layer 2/3.(a) Radial distribution of mean dF/F response to the PW (green) and to the sum of the two closest adjacent whiskers (black). ***Mann-Whitney P=8.1 × 10−4 for PW and *P=0.024 for adjacent whiskers. (b) A simple model of the projections to the barrel and septal compartments. A supra-linear integration of VPm-head and VPm-core inputs during correlated stimulation may occur in neurons above the barrel-septa border that receive both inputs, while neurons above barrel centre and septum centre mainly receive a single source of input and are therefore not subjected to the same mechanism. Bar., barrel.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5121329&req=5

f5: A model of multi-whisker supra-linear integration in barrel cortex layer 2/3.(a) Radial distribution of mean dF/F response to the PW (green) and to the sum of the two closest adjacent whiskers (black). ***Mann-Whitney P=8.1 × 10−4 for PW and *P=0.024 for adjacent whiskers. (b) A simple model of the projections to the barrel and septal compartments. A supra-linear integration of VPm-head and VPm-core inputs during correlated stimulation may occur in neurons above the barrel-septa border that receive both inputs, while neurons above barrel centre and septum centre mainly receive a single source of input and are therefore not subjected to the same mechanism. Bar., barrel.
Mentions: Our study provides evidences for the existence of two maps, for correlated and anti-correlated stimulation-preferring neurons, both with a ring shape above the barrel–septum border. We showed that they spatially correspond to locations where supra-linearity properties dominate, allowing the boost of cell responses to synchronous multi-whisker activation. Why would the supra-linearity be located above the barrel–septum border, building a correlation map that largely escapes the area above barrel? It may arise from integration at multiple stages of the thalamo-cortical loop10 as well as from local cortical processing. On the basis of our observations, we propose a cortical model of supra-linear integration of multi-whisker inputs. Thalamic inputs to layer 2/3 neurons have three main origins: (i) mono-whisker inputs come from VPm-core in layer 4 barrels, and are then vertically relayed to layers 2/3. (ii) Multi-whisker inputs are conveyed by VPm-head11 to layer 4 septa, and then again vertically relayed to layers 2/3 (ref. 12). (iii) Multi-whisker inputs can also originate in POm and reach layer 1, where it connects to layer 2/3 dendritic arbors. However, recent studies have shown that in anaesthetized animals sensory transmission through this nucleus is often strongly diminished or impeded by feed-forward inhibition from the zona incerta1314. Because of their uneven distribution above barrel and septa, the pathways (i) and (ii) could contribute to the emergence of the map. The spatial profile of the response to deflections of the PW is centred on the corresponding barrel, due to VPm-core inputs. VPm-head inputs centre the response to surrounding whiskers above the septa, as observed in Fig. 5a, where the radial distribution of the responses to PW and to the sum of two closest adjacent whiskers is plotted. Depending on their location, neurons in layer 2/3 could thus have three patterns of input (Fig. 5b): mainly mono-whisker (PW) inputs above barrels; mainly multi-whisker inputs above septa; and a combination of both above the border between barrel and septa. In the case of layer 2/3 neurons above the barrel–septa border, supra-linear summation of PW and surround inputs during correlated or anti-correlated stimulations could then occur, through nonlinear dendritic integration1516. Figure 5b illustrates the expected profile of the supra-linearity. This model predicts a map for correlation-preferring neurons with a ring shape aligned vertically with each barrel border, differing from the simple two-component (barrel and septa) domains, and the existence of a nonlinear cortical integration in the multi-whisker processing that should appear to be non-uniform above barrel and septa. The same mechanism could account for the map for anti-correlation-preferring neurons.

View Article: PubMed Central - PubMed

ABSTRACT

In the barrel cortex, several features of single-whisker stimuli are organized in functional maps. The barrel cortex also encodes spatio-temporal correlation patterns of multi-whisker inputs, but so far the cortical mapping of neurons tuned to such input statistics is unknown. Here we report that layer 2/3 of the rat barrel cortex contains an additional functional map based on neuronal tuning to correlated versus uncorrelated multi-whisker stimuli: neuron responses to uncorrelated multi-whisker stimulation are strongest above barrel centres, whereas neuron responses to correlated and anti-correlated multi-whisker stimulation peak above the barrel–septal borders, forming rings of multi-whisker synchrony-preferring cells.

No MeSH data available.