JOURNALOF NEUROPHYSIOLOGY Vol. 70, No. 5, November 1993. Printed in U.S.A. Development of Metabolic Activity Patterns in the Somatosensory Cortex of Cats SHARON L. JULIANO, REBECCA A. CODE, MARK TOMMERDAHL, AND DON E. ESLIN Department of Anatomy and Cell Biology and Neuroscience, Uniformed Services University of the Health Sciences, Bethesda, Maryland 20814; and Department of Physiology, University of North Carolina, Chapel Hill, North Carolina 2 75 14 SUMMARY AND CONCLUSIONS 1. The development of cortical responses to somatic stimula- INTRODUCTION tion was studied in kittens 2-5 wk of age using the 2-deoxyglucose (2DG) technique. During the 2DG experiment each kitten re- ceived an innocuous intermittent vertical displacement stimulus to the forepaw. 2. The pattern of metabolic activity was substantially different in young animals compared with adults. In the individual autora- diographs of the 2-wk-old kittens stimulus-evoked 2DG uptake in primary somatosensory cortex was localized to a small spot in the upper portion of the cortex, whereas in the adult the label ex- tended vertically through the cortical layers and appeared more columnlike. Individual patches of label were substantially smaller and lessdense in young animals. Over a period of several weeks the evoked activity evolved to the more extensive adult pattern. The 2DG uptake displayed a mature distribution by -4-5 wk of age. During this period, the cortical architecture also evolved from an immature to a mature arrangement. Although it is becoming clear that early experience is im- portant in establishing functional and anatomic relations in the adult brain, very little is known about how the neonatal brain responds to stimulation. The development of physio- logical activity has been assessed to some extent in the vi- sual system, where a number of studies describe early activ- ity in the visual cortex (see Armstrong-James and Fox 1988 for review). These experiments report the ontogeny of vi- sual cortical responses and indicate that although develop- ing neocortex responds in a visuotopic manner to stimula- tion of the receptor sheet, many neuronal properties remain immature up to 6-7 wk of age. For example, the receptive fields of neurons in the visual cortex are larger in young cats than adults and the individual visual neurons of kittens do not display the diversity of response properties that are pres- ent in adult (see Armstrong-James and Fox 1988 for re- 3. The evoked activity was reconstructed into two-dimensional maps; the distribution of label ~1.5 SD above background was considered to be stimulus related. In the adult, the pattern ap- peared as a strip or strips of increased metabolic activity that ex- view). tended in the rostrocaudal direction for - 1 mm. In contrast, the activity pattern in animals 2-4 wk old was less discretely organized into “strips” and was more diffusely spread over several mms of somatosensory cortex. The two-dimensional pattern gradually co- alesced into a more localized strip by -4-5 wk of age. Although the pattern of label was more widespread in the young animals, the absolute distance of the spread of activity did not vary substan- tially, regardless of the age of the animal. The development of connections to and within the neo- cortex has also been described in the visual system. Both the thalamocortical and intrinsic cortical connections of pri- mary visual cortex undergo dramatic alterations during maturation. In the adult cat, the thalamocortical termina- tions have a distinctly patchy distribution related to eye- specific ocular dominance columns (Hubel and Wiesel 4. Other measurements regarding the distribution of activity at different ages indicate that the amount of cortex activated in- creases in absolute terms, although the percent of cortex activated by the stimulus decreases. The overall intensity of the 2DG uptake as measured on the two-dimensional maps increases with age, as does the variability of the 2DG uptake; a wider range of intensity values is seen in the adult. Plots created from the individual two- dimensional reconstructions allowed a measure of “patch strength” at different ages. These histograms relate the most in- tense region of uptake in a given map to the spatial distribution of activity spreading in the medial and lateral directions. The infor- mation obtained from these plots provides evidence that the indi- vidual patches of 2DG uptake gain strength (i.e., intensity of la- bel) as the somatosensory cortex matures. 1972). The intrinsic connections are also obviously patch- like, although the functional significance of the individual patches is not as clear as the thalamocortical patches, which 5. We suggest that the pattern of activity seen in response to somatic stimulation in developing cats is underlined by evolving structural and neural patterns identified in visual and somatosen- sory cortex of maturing kittens. The amount of 2DG uptake in young animals is lessdense and covers a greater fraction of cortex compared with the adult pattern, which is more organized and coalesced into discrete units. are related to a specific eye (Gilbert 1983; Gilbert and Wie- se1 1983, 1989). The axons of the developing thalamocorti- cal projections are initially less discrete and gradually orga- nize over a period of several weeks into precise patchlike structures that terminate in layer 4 (Katz and Callaway 1992; Luhmann et al. 1990). In addition, the tangential or horizontal connections within visual cortex undergo elabo- rate refinements, beginning with a complete lack of specific clustering at birth and evolving to highly formed clusters of cells (Katz and Callaway 1992). It is likely that the ontog- eny of the anatomic changes occurring in visual cortex is reflected in functional changes leading to neurons that pos- sess smaller receptive fields, are more specifically domi- nated by input from one eye, and are driven by specific features indicative of visual cortical neurons. Similar structure-function correlations describing the evolution of neural activity and anatomic relations are not 2117