Sensory inputs from whisking movements modify cortical whisker maps visualized with functional magnetic resonance imaging

Abstract

Rodents vary the frequency of whisking movements during exploratory and discriminatory behaviors. The effect of whisking frequency on whisker cortical maps was investigated by simulating whisking at physiological frequencies and imaging the whisker representations with blood oxygen level-dependent (BOLD) functional magnetic resonance imaging. Repetitive deflection of many right-sided whiskers at 10 Hz evoked a positive BOLD response that extended across contralateral primary somatosensory cortex (SI) and secondary somatosensory cortex (SII). In contrast, synchronous deflection of 2 adjacent whiskers (right C1 and C2) at 10 Hz evoked separate positive BOLD responses in contralateral SI and SII that were predominantly located in upper cortical layers. The positive BOLD responses were separated and partially surrounded by a negative BOLD response that was mainly in lower cortical layers. Two-whisker representations varied with the frequency of simulated whisking. Positive BOLD responses were largest with 7-Hz deflection. Negative BOLD responses were robust at 10 Hz but were weaker or absent with 7-Hz or 3-Hz deflection. Our findings suggest that sensory inputs attributable to the frequency of whisking movements modify whisker cortical representations.

Figure 1

Imaging whisker representations with fMRI. (A) Schematic of the whiskers on the right side of a rat’s snout. Whisker rows are labelled A - E whereas whisker arcs (running dorso-ventrally) are numbered. Outlying whiskers, which are found between whisker rows at the caudal end of the whisker pad, have not been labelled for simplicity. Filled red circles denote the C1 and C2 whiskers. (B) Orientation of the whisker actuator in the scanner. A transmit and receive coil lies on top of the rat’s head. (C) Schematic illustrating the relative position of SI, SII and parietal ventral (PV) whisker representations in a coronal slice approximately 2.5 mm caudal to bregma that cuts through the left C1/C2 whisker barrels in SI (adapted from Chapin and Lin 1984; Hoffer and others 2003; Benison and others 2007). Whisker barrel rows run in and out of the plane of the slice. Red ellipses denote the positions of the cortical columns in SI and SII receiving principal whisker input from C1/C2 whiskers. The relative positions of the whisker barrel columns (A - E) are given for SI (SI wh) and SII (SII wh). SI f/tr denotes the forelimb/trunk representation that lies medial to the SI whisker map. rhf signifies the rhinal fissure.

Figure 2

BOLD signal evoked by 10 Hz deflection of either two whiskers or many whiskers in multiple whisker rows in the same animal. (Ai) Schematic shows whisker trim used for two-whisker protocol. Red circles denote the follicles of deflected whiskers. Empty circles indicate trimmed whiskers. Filled circles represent untrimmed whiskers that were not deflected. (Aii) Single-animal map of the BOLD responses evoked by two-whisker deflection. Pseudocoloured voxels have a positive BOLD (red) or negative BOLD (blue) signal that is significantly different from baseline. The pseudocolour scale bars apply to both Aii and Bii. Numbers denote the rostro-caudal distance of each slice from bregma. (Bi) Schematic shows whisker trim used for multiple whisker-row protocol. Whisker colour code as per A. (Bii) Map of the BOLD responses evoked by multiple whisker-row deflection for the animal used in A. Pseudocoloured voxels have a positive BOLD (red) or negative BOLD (blue) signal that is significantly different from baseline. For simplicity, only slices with positive or negative BOLD signal are shown in Aii and Bii.

Figure 3

Whisker representations depend on the number of deflected whiskers. (Ai) Schematic of two-whisker deflection protocol. (Aii) Group map (n = 8) of the BOLD responses evoked by the right C1 and C2 whiskers. Pseudocoloured voxels have a positive BOLD (red) or negative BOLD (blue) signal that is significantly different from baseline. The pseudocolour scale bars apply to both Aii and Bii. Statistical parametric maps in Fig. 2 use the same scale to enable comparison. (Bi) Schematic of multiple whisker-row protocol. (Bii) Group map (n = 8) of the BOLD responses evoked by deflection of multiple whisker rows on the left side of the snout. Pseudocoloured voxels have a positive BOLD (red) or negative BOLD (blue) signal that is significantly different from baseline.

Figure 4

Deflection of many whiskers evokes a larger positive BOLD response in SI and SII than two-whisker deflection. (A) Amplitudes of the positive BOLD responses in SI evoked by the two-whisker and multiple row deflection protocols in the same animals. (B) Amplitudes of the positive BOLD responses in SII evoked by the two-whisker and multiple row deflection protocols in the same animals. (C) Volumes of the positive BOLD responses in SI evoked by the two-whisker and multiple row deflection protocols in the same animals. (D) Volumes of the positive BOLD responses in SII evoked by the two-whisker and multiple row deflection protocols in the same animals.

Figure 5

Single-animal maps of the BOLD signal evoked by right C1 and C2 whisker deflection at 3 Hz (A), 7 Hz (B) and 10 Hz (C). The rostro-caudal position of each slice with respect to bregma is given. Pseudocoloured voxels have a positive BOLD (red) or negative BOLD (blue) signal that is significantly different from baseline. The pseudocolour scale bar applies to all maps.

Figure 6

Whisker representations in neocortex depend on deflection frequency. (A) Group map (n = 7) of BOLD responses evoked by 3 Hz deflection of right C1 and C2 whiskers. Numbers denote the rostro-caudal position of each slice with respect to bregma. A line drawing from a rat atlas is superimposed on the slice 2.5 mm caudal to bregma. Pseudocoloured voxels have a positive BOLD (red) or negative BOLD (blue) signal that is significantly different from baseline. (B) Group map (n = 7) of BOLD responses evoked by 7 Hz deflection of right C1 and C2 whiskers arranged as in A. (C) Group map (n = 8) of BOLD responses evoked by 10 Hz deflection of right C1 and C2 whiskers arranged as in A. The pseudocolour scale bar applies to all maps.

Figure 7

Single-animal analysis of two-whisker BOLD representations. (A) Regions of interest and the line drawing from a rat atlas are superimposed on a brain slice. The colour code (red, positive BOLD; blue, negative BOLD) denotes the principal BOLD response in each region of interest. (B) Volume and amplitude of the positive BOLD response (PBR) are correlated. (C) Change in BOLD signal in SI (filled circles) and SII (open circles) with varying whisker deflection frequency. Error bars denote SEM. (D) Maximum BOLD signal intensities in SI and SII. The dashed line is the unity line. (E) Number of voxels in the SI positive BOLD response and SII positive BOLD response. The dashed line is the unity line.

Figure 8

Relationship between positive and negative BOLD responses in SI. (A) Schematic of an image slice through whisker barrel cortex. A dashed line splits SI into upper (L1 - L4) and lower (L5 - L6) cortical layers. Red, positive BOLD response. Blue, negative BOLD response. (B) Volumes of the positive and negative BOLD responses in L1 - L4 and L5 - L6 of SI.