The Nature of the Sensory Input to the Neonatal Rat Barrel Cortex

Abstract

Sensory input plays critical roles in the development of the somatosensory cortex during the neonatal period. This early sensory input may involve: (1) stimulation arising from passive interactions with the mother and littermates and (2) sensory feedback arising from spontaneous infant movements. The relative contributions of these mechanisms under natural conditions remain largely unknown, however. Here, we show that, in the whisker-related barrel cortex of neonatal rats, spontaneous whisker movements and passive stimulation by the littermates cooperate, with comparable efficiency, in driving cortical activity. Both tactile signals arising from the littermate's movements under conditions simulating the littermates' position in the litter, and spontaneous whisker movements efficiently triggered bursts of activity in barrel cortex. Yet, whisker movements with touch were more efficient than free movements. Comparison of the various experimental conditions mimicking the natural environment showed that tactile signals arising from the whisker movements with touch and stimulation by the littermates, support: (1) a twofold higher level of cortical activity than in the isolated animal, and (2) a threefold higher level of activity than in the deafferented animal after the infraorbital nerve cut. Together, these results indicate that endogenous (self-generated movements) and exogenous (stimulation by the littermates) mechanisms cooperate in driving cortical activity in newborn rats and point to the importance of the environment in shaping cortical activity during the neonatal period.

Significance statement: Sensory input plays critical roles in the development of the somatosensory cortex during the neonatal period. However, the origins of sensory input to the neonatal somatosensory cortex in the natural environment remain largely unknown. Here, we show that in the whisker-related barrel cortex of neonatal rats, spontaneous whisker movements and passive stimulation by the littermates cooperate, with comparable efficiency, in driving cortical activity during the critical developmental period.

Keywords: EEG; barrel; development; neonate; whisker.

Figure 1.

Whisker movement patterns in neonatal rats. A, Snapshot of a P5 rat snout with the whisker tips marked with a black paint. Example trace (B) and cross-correlation coefficients (C) of movement of the four whiskers labeled on A. D, Time-colored traces of the whisker movements marked with asterisks on B. Gray circles represent the whisker bases. E, F, Histograms of whisker movement direction (E) and angular amplitude (F). Pooled data from 10 nonanesthetized P2–P7 rat pups (in total 675 movements).

Figure 2.

Activity in a cortical barrel of a neonatal rat during free principal whisker movements and active touch. A, The color-coded example traces of caudally directed free movement of C1 and C2 whiskers (top left) and a movement associated with C1 whisker contact with an external object (top right) obtained from a P4 nonanesthetized rat pup. Bottom, Corresponding movement amplitude vectors and the result of their subtraction (ΔC1–C2). The color encodes the time between the movement onset and the end. Bottom, Simultaneous LFP (black traces) and MUA (red bars) recordings from L4 of C1 barrel column. Vertical dashed lines indicate movement onsets. B, Corresponding wavelet LFP spectrograms from L4 of the C1 cortical barrel column. C, D, Caudal C1 whisker movement-triggered C1 L4 layer (C) spike raster plots and (D) cumulative distribution of spikes detected within 1 s after C1 movement onset. E–G, Group data from five nonanesthetized P4–P7 rats on the (E) spike firing rate (F) total spike counts and (G) LFP power in α/β and γ frequency bands in L4 of principal barrel column evoked by free PW movements and movements with touch. Baseline MUA and LFP power was assessed within 1 s of baseline average. *p < 0.05.

Figure 3.

Cortical activity in the principal barrel column during artificial whisker movements. A, Schematic drawing of motor facial nerve stimulation evoked protractions: (left) free and (right) with an object introduced in the whisker path and corresponding examples of time color-coded D2 whisker movement trajectories in a urethane-anesthetized P6 rat. B, Schematic drawing of electrodes placement for stimulation of the middle branch (BS, ramus buccolabialis superior) of the facial nerve. C, Example responses evoked by artificial whisker movements in L4 of the D2 cortical barrel column. D, The stimulus-triggered averages (n = 100) of LFP (black traces) overlaid on color-coded CSD plot and (E) MUA peristimulus time histograms across layers. F–H, Statistical plots of (F) L4 MUA peristimulus time histograms during free and touching artificial movements (SEP) and (G) brief PW deflection, and (H) parameters of the artificial whisker movement-evoked responses in the cortical L4 normalized to the PW deflection-evoked responses. F–H, Pooled data from four urethane-anesthetized P5–P6 rats. *p < 0.05. ns, Not significant.

Figure 4.

Activation of cortical barrels during littermate movements. A, Littermate (left) is placed snout to snoutpad to the recorded head-restrained P3 rat pup (right). Both animals are nonanesthetized. B, Example response evoked by the littermate head movement (top) in the L4 of a C1 cortical column (middle) and the corresponding wavelet spectrogram (bottom). C, Movement onset triggered spike raster plot in L4 of a C1 barrel column. D–F, Group data on (D) littermate movement triggered L4 MUA time histograms (bottom, movements duration), (E) total spike counts, and (F) L4 LFP power in α-β and γ frequency bands within a 1 s period before and after littermate's movements. D–F, Pooled data from six pairs of P2–P6 nonanesthetized rats. G, Overall L4 MUA frequency in the barrel cortex in nonanesthetized rat pups during free whisking, continuous PW contact with the passive objects (fur, mesh, anesthetized littermate), and a PW contact with the nonanesthetized littermate normalized to the level of activity after deafferentation by cutting the ION. Bottom, Color-coded p value map for statistical comparisons between different conditions. *p < 0.05; **p < 0.01. ns, Not significant.