Whisker maps in marsupials: Nerve lesions and critical periods

Abstract

In the wallaby, whisker-related patterns develop over a protracted period of postnatal maturation in the pouch. Afferents arrive simultaneously in the thalamus and cortex from postnatal day (P) 15. Whiskerrelated patterns are first seen in the thalamus at P50 and are well formed by P73, before cortical patterns first appear (P75) or are well developed (P85). This study used the slow developmental sequence and accessibility of the pouch young to investigate the effect of nerve lesions before afferent arrival, or at times when thalamic patterns are obvious but cortical patterns not yet formed. The left infraorbital nerve supplying the whiskers was cut at P0 -93 and animals were perfused at P112-123. Sections through the thalamus (horizontal plane) and cortex (tangential) were reacted for cytochrome oxidase to visualize whisker-related patterns. Lesions of the nerve at P2-5, before innervation of the thalamus or cortex, resulted in an absence of patterns at both levels. Lesions from P66 -77 also disrupted thalamic and cortical patterns, despite the fact that thalamic patterns are normally well established by P73. Lesions from P82-93 resulted in normal thalamic and cortical patterns. Thus, despite the wallaby having clearly separated times for the development of patterns at different levels of the pathway, these results suggest a single critical period for the thalamus and cortex, coincident with the maturation of the cortical pattern. Possible mechanisms underpinning this critical period could include dependence of the thalamic pattern on corticothalamic activity or peripheral signals to allow consolidation of thalamic barreloids. © 2006 Wiley-Liss, Inc. Key words: trigeminal pathway; vibrissa; barrel; somatosensory development; whisker folliclesThe rodent whisker-barrel pathway has provided a model system par excellence for studies of normal somatosensory development and function as well as plasticity after lesioning (Miller et al., 2001;Waite, 2004). The pattern of whiskers on the muzzle is replicated in visible and quantifiable patterns at each level of the neuraxis from brainstem to cortex. Moreover, the patterns develop in a temporal sequence from periphery to somatosensory cortex. The whiskers on the muzzle are visible from embryonic day (E) 14 in the rat, with whisker-related patterns appearing first in the brainstem [E20 to postnatal day (P) 0 -1], then the thalamus (P2-3) and cortex (P3-5) (Killackey, 1985). During this developmental period, pattern development is vulnerable to peripheral lesions, such as removal of the whisker follicles or section of their sensory nerve, the infraorbital. Peripheral lesions in the perinatal period cause death of many trigeminal ganglion cells and permanent loss of patterns in the brainstem nuclei.

The evolution of active vibrissal sensing in mammals: evidence from vibrissal musculature and function in the marsupial opossumMonodelphis domestica

“…The layout of the opossum mystacial pad is quite similar to that of the wallaby (Waite et al, 2006) as there seem to be four rows of vibrissae in both species, with two nasal whiskers present in the dorsal-most row. Weller (Weller, 1993) also found two dorsal-most whiskers in brush-tailed opossums; however, that study reported six rows of whiskers in total (or five if their row A is labelled as nasal whiskers).…”

Development of structural and functional connectivity in the thalamocortical somatosensory pathway in the wallaby

“…In the wallaby there is a clear increase in the non‐NMDA to NMDA ratio during development, suggesting that there are no major differences in the pattern of maturation of glutamatergic synaptic transmission between the species. There may, however, be differences in the relative timings of these events which may in turn correlate with the observation that the critical period for pattern formation in the cortex (as visualized using mitochondrial enzymes which can reflect organization of pre and/or postsynaptic strucutures) terminates during the period that patterns form in the wallaby (Waite et al ., 2006) but in mice has been reported to extend beyond it to P5 (Woolsey et al ., 1979). It would also be of interest to determine whether there are differences in the downstream signalling pathways which mediate developmental plasticity in the somatosensory cortex of mice and wallabies.…”

“…It is tempting to speculate that the appearance of the fast, non‐NMDA‐dominated component, which we suggest may be required to produce firing of postsynaptic neurons, is necessary to drive pattern formation. The time at which the non‐NMDA‐mediated component becomes dominant also correlates with the end of the critical period for pattern formation in the somatosensory thalamus and cortex of the wallaby as visualized with cytochrome oxidase (Waite et al ., 2006).…”

“…While there are clear cellular clusters associated with the whiskers in wallaby brainstem (Waite et al ., 1994) and thalamus (Leamey et al ., 1996), and segregation of thalamocortical axons in developing animals, there are no cellular clusters present in the somatosensory cortex at any stage of development (Waite et al ., 1991, 2006). This is consistent with a number of studies in mice which have demonstrated that the clustering of pre‐ and postsynaptic elements in the somatosensory cortex is mediated by different processes.…”

What can whiskers tell us about mammalian evolution, behaviour, and ecology?

“…2b). These structures have been detected in some rodents (mice, rat, hamster Cricetus cricetus; Woolsey et al 1975), marsupials (wallaby Macropus eugenii; Woolsey et al 1975, Waite et al 2006, pinnipeds (California sea lion Zalophus californianus; Sawyer et al 2016), and nocturnal primates (northern greater galago Otolemur garnettii; Sawyer et al 2015), but are absent in the guinea pig Cavia porcellus and beaver Castor fiber (Woolsey et al 1975), and many species have not yet been investigated. This one-to-one mapping of whisker signals ascending through the brain to somatosensory cortex has inspired many neuroscientists to use this system as a model of mammalian sensory processing, since signals can be traced from the whisker to the cortex.…”