Effects of neonatal whisker lesions on mouse central trigeminal pathways

Abstract

The mystacial vibrissae or whiskers on the face have a large representation in the rodent central nervous system. In rats and mice the projections arising from each vibrissa can be demonstrated histologically in five separate parts of the central trigeminal pathway. At every location, the pattern of the projections is isomorphic to the pattern of the facial vibrissae. For example, in the somatosensory cortex (SmI), multicellular cytoarchitectonic units in layer IV--termed barrels--correspond anatomically and functionally to the contralateral whiskers. The cortical barrels are absent at birth and their cytoarchitectonic pattern can be altered by neonatal whisker lesions. The effect is graded such that whisker damage on or after postnatal day (PND) 6 does not produce changes in the anatomical somatotopy. We undertook the present study to determine whether similar "critical periods" for susceptibility to vibrissa damage exist in the subcortical trigeminal stations of mice. In particular, we wished to find out whether subcortical projections are susceptible to whisker damage in a sequence which parallels other described developmental sequences, as has been concluded from previous work on the mouse (Woolsey et al., '79), or whether the "critical periods" are related to other aspects of development as has been concluded from work on the rat (Belford and Killackey, '80). Neonatal Swiss Webster mice sustained lesions of a single row of whiskers on PND 1, 2, 3, 4, or 5. The animals survived to adulthood. Their brains were sectioned and stained for the mitochondrial enzyme, succinic dehydrogenase (SDH), which demonstrates whisker somatotopy in all central nervous system (CNS)stations. The whisker representations at each level of the pathway, often in the same individual, were reconstructed from serial sections to assess qualitative and quantitative changes in somatotopy. Histological sections through the faces of the experimental animals were used to determine the extent of whisker damage and to show that few nerve fibers innervate the damaged zone on the face. In the brainstem representations, the zones corresponding to the damaged whiskers are shrunken and pale, regardless of the animal's age at vibrissa damage; this probably reflects the degeneration of the primary afferents. In the thalamus and the cortex, whisker damage at later postnatal times has progressively less effect on the anatomical projections patterns. Based on the changes in the projection patterns related to the damaged vibrissae and the changes in the projection patterns related to the remaining, intact vibrissae,(ABSTRACT TRUNCATED AT 400 WORDS)

The representation of peripheral nerve inputs in the S-I hindpaw cortex of rats raised with incompletely innervated hindpaws

“…With respect to young animals, if the previously discussed relationship between cortical reorganization and peripheral template disruption is correct, patterns of cortical recovery after early injuries could differ because of variable template disruptions after different injuries. Consistent with this line of thinking, the disruption in the spatial partitioning of cells and fibers at cortical levels after whole nerve transection differs from the disruption produced after cauterization of distal nerve endings (e.g., compare Durham and Woolsey, 1984;Jeanmonod et al, 198 1;andBelford, 1979, with Bates et al, 1982;Killackey and Shinder, 198 1;. This difference appears to be related to the different consequences of these injuries on the central terminations of injured primary sensory fibers (e.g., Bates et al, 1982;Erzurumlu and Killackey, 1982;Killackey and Shinder, 198 1).…”

“…In normal rodents, the vibrissae follicles are represented by spatially parcelled groups of neurons at brain stem, thalamic, and cortical levels of the trigeminal neuraxis (Belford and Killackey, 1979b;Erzurumlu et al, 1980;Ivy and Killackey, 1982;Killackey, 1973;Van der Loos, 1976;Woolsey and Van der Loos, 1970;Woolsey et al, 1979). Cauterization of follicles or injury of the infraorbital nerve during the first several postnatal days results in (1) loss of primary sensory neurons and disruption of the cellular organization in the trigeminal ganglion (Bates and Killackey, 1984;Durham and Woolsey, 1984;Killackey, 1982, 1983;Jacquin and Rhoades, 1983;Math et al, 1984;Rhoades et al, 1983;Savy et al, 1981;Waite, 1984;Waite and Cragg, 1979); (2) disorganization and shrinkage of brain stem trigeminal nuclei due to transynaptic loss of neurons (Waite, 1984); (3) abnormal spatial patterns of cells and fiber terminals at synaptic relays in the brain stem (Bates and Killackey, 1984;Bates et al, 1982;Killackey, 1979a, b, 1980;Durham and Woolsey, 1984;Erzurumlu and Killackey, 1983;Jacquin and Rhoades, 1983;Killackey and Shinder, 1981;Rhoades ef. al., 1983); thalamus Killackey, 1979a, b, 1980;Durham and Woolsey, 1984;Killackey and Shindler, 1981;Woolsey et al, 1979) and S-I cortex Durham and Woolsey, 1984;Jeanmonod et al, 1977, 198 1;Jensen and Killackey, 1984;Belford, 1979, 1980;K...…”

“…Cauterization of follicles or injury of the infraorbital nerve during the first several postnatal days results in (1) loss of primary sensory neurons and disruption of the cellular organization in the trigeminal ganglion (Bates and Killackey, 1984;Durham and Woolsey, 1984;Killackey, 1982, 1983;Jacquin and Rhoades, 1983;Math et al, 1984;Rhoades et al, 1983;Savy et al, 1981;Waite, 1984;Waite and Cragg, 1979); (2) disorganization and shrinkage of brain stem trigeminal nuclei due to transynaptic loss of neurons (Waite, 1984); (3) abnormal spatial patterns of cells and fiber terminals at synaptic relays in the brain stem (Bates and Killackey, 1984;Bates et al, 1982;Killackey, 1979a, b, 1980;Durham and Woolsey, 1984;Erzurumlu and Killackey, 1983;Jacquin and Rhoades, 1983;Killackey and Shinder, 1981;Rhoades ef. al., 1983); thalamus Killackey, 1979a, b, 1980;Durham and Woolsey, 1984;Killackey and Shindler, 1981;Woolsey et al, 1979) and S-I cortex Durham and Woolsey, 1984;Jeanmonod et al, 1977, 198 1;Jensen and Killackey, 1984;Belford, 1979, 1980;Killackey et al, 1976;Van der Loos and Woolsey, 1973;Waite and Cragg, 1979;Weller and Johnson, 1975;Woolsey and Wann, 1976); and (4) alterations in the dendritic organization of cortical cells (Harris and Woolsey, 1979, 198 1;Ryugo et al, 1975;Steffen and Van der Loos, 1980). These studies clearly indicate that the rodent somatosensory system is in a formative stage during the...…”

“…These studies clearly indicate that the rodent somatosensory system is in a formative stage during the first several postnatal days and that spatial partitioning of connections involves an "outside-in" or peripheral-to-central sequence. The relative time relationships for partitioning at successively higher central levels of the system remain controversial, but there is agreement that the infraorbital nerve acts as a primary template for patterns at higher levels of the neuraxis (e.g., Durham and Woolsey, 1984;Killackey, 1982, 1983;Jeanmonodet al, 198 1;Killackey, 1985;Van der Loos and Do& 1978;Van der Loos and Welker, 1985). Neonatal peripheral injury disrupts this template and consequently the structural organization of ascending central connections undergoes an abnormal initial development.…”

Somatosensory cortical plasticity: recruiting silenced barrels by active whiskers

“…Whisker-specific patterning of thalamocortical axon terminals and modular organization of layer IV granule cells around these patches (barrels) develop postnatally . Morphological and functional organizations of the barrel fields are permanently altered if the whiskers or the infraorbital nerve innervating them are damaged before the first 4 days after birth (Belford and Killackey, 1980;Durham and Woolsey, 1984;Van der Loos and Woolsey, 1973;Woolsey and Wann, 1976). Thus, the structural organization of the barrel fields is highly sensitive to peripheral injury during a well-defined critical period in development.…”