Protracted Development of Responses to Whisker Deflection in Rat Trigeminal Ganglion Neurons

Abstract

Shoykhet, Michael, Pranav Shetty, Brandon S. Minnery, and Daniel J. Simons. Protracted development of responses to whisker deflection in rat trigeminal ganglion neurons. J Neurophysiol 90: 1432-1437. First published June 11, 2003 10.1152/jn.00419.2003. The rodent whisker-to-barrel pathway constitutes a major model system for studying experience-dependent brain development. Yet little is known about responses of neurons to whisker stimulation in young animals. Response properties of trigeminal ganglion (NV) neurons in 2-, 3-, and 4-week-old and adult rats were examined using extracellular single-unit recordings and controlled whisker stimuli. We found that the receptive field size of NV neurons is mature in 2-week-old animals while response latencies, magnitudes, and angular tuning continue to develop between 2 weeks of age and adulthood. At the earliest time recorded, NV neurons respond to stimulation of only one whisker and can be characterized as slowly or rapidly adapting (SA, RA). The proportion of SA and RA neurons remains constant during development. Consistent with known on-going myelination of NV axons, response latencies decrease with age, becoming adult-like during the third and fourth postnatal weeks for RA and SA neurons, respectively. Unexpectedly, we found that evoked response magnitudes increase several-fold during development becoming adult-like only during the fourth postnatal week. In addition, RA neurons become less selective for whisker deflection angle with age. Maturation of response magnitude and angular tuning is consistent with developmental changes in the mechanical properties of the whisker, the whisker follicle, and the surrounding tissues. The findings indicate that whiskerderived tactile inputs mature during the first postnatal month when whisker-related cortical circuits are susceptible to long-term modification by sensory experience. Thus normal developmental changes in sensory input may influence functional development of cortical circuits.

Conversion of Functional Synapses into Silent Synapses in the Trigeminal Brainstem after Neonatal Peripheral Nerve Transection

“…In the PrV, barrelette cells receive inputs from whisker-specific trigeminal ganglion cells, which show either lowfrequency spontaneous or high-frequency sensory activities (Minnery and Simon, 2003;Shoykhet et al, 2003). If silent synapses are a consequence of the absence of high-frequency sensory inputs, then highfrequency electrical stimulation of the afferent pathway could convert silent synapses into functional synapses.…”

“…More recent studies uncovered that trigeminal ganglion cells have TTXresistant Na ϩ and voltage-dependent Ca 2ϩ channels that produce Ca 2ϩ spikes (Kim and Chung, 1999;Cabanes et al, 2002). Furthermore, TTX or bupivacaine does not appear to block spontaneous activity of trigeminal ganglion cells Shoykhet et al, 2003). In contrast to pharmacological activity blockade experiments, gene deletion or alteration studies in mice showed that disruption of NMDA receptor subunits NR1 or NR2B prevent development of barrelette patterns altogether (Li et al, 1994;Kutsuwada et al, 1996;Iwasato et al, 1997).…”

Stimulus-Dependent Changes in Spike Threshold Enhance Feature Selectivity in Rat Barrel Cortex Neurons

“…In the barrel cortex of rodents, neurons are selective for the angular direction in which their corresponding mystacial whisker [the principal whisker (PW)] is deflected (Simons, 1983;Simons and Carvell, 1989;Bruno and Simons, 2002). Direction selectivity is already present in the principal trigeminal nucleus Shoykhet et al, 2003) and in the ventrobasal nucleus of the thalamus (Simons and Carvell, 1989;Bruno et al, 2003;Timofeeva et al, 2003). Therefore, the spike output tuning of individual barrel cortex cells may simply be a faithful reproduction of the tuning properties of their synaptic inputs, or, alternatively, postsynaptic mechanisms may transform a broadly tuned synaptic input into a sharply tuned spike output.…”

Adaptation of trigeminal ganglion cells to periodic whisker deflections

“…Responses of rapidly adapting cutaneous receptors are moderately affected by tissue viscoelasticity (Grigg et al 2004). In the vibrissa system, trigeminal ganglion neurons fire progressively more robustly during the first postnatal month, presumably reflecting changes in the mechanical properties of the facial tissue (Shoykhet et al 2003), and in adult animals paralyzed by neuromuscular blockade the lack of facial muscle tone often leads to the failure of a deflected whisker to return autonomously to its neutral position following whisker displacement (Minnery and Simons 2003). Here we examine further possible effects of tissue compliance by comparing responses of trigeminal ganglion neurons recorded separately during experiments in which animals were or were not subject to neuromuscular blockade.…”