Effects of neonatal whisker lesions on mouse central trigeminal pathways

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, we conclude that each central vibrissal representation has a temporally different “critical period.” The critical period ends first in the brainstem, next in the thalamus, and last in the cortex. These data, suggest a peripheral-to-central sequence in the development of somatotopic patterns in the pathway, such that a given station might “instruct” the next more central one. Two other lines of evidence are consistent with this conclusion: the order in which neurons in the pathway are generated and the order in which each part of the pathway differentiates to an adult morphology, which both have a similar “outside-to-in” sequence.