Developmental changes in odor-evoked activity in rat piriform cortex.

In adult rats, odor-evoked Fos protein expression is found in rostrocaudally-oriented bands of cells in anterior piriform cortex (APC), likely indicating functionally distinct subregions, while activated cells in posterior piriform cortex (PPC) lack apparent spatial organization. To determine whether these patterns are present during early postnatal life, and whether they change during development, Fos expression was assessed following acute exposure to single aliphatic acid odors in developing rats beginning at postnatal day 3 (P3). In the olfactory bulb, Fos-immunoreactive cells were present in the granule cell, mitral cell and glomerular layers at the earliest ages examined. Cells immunopositive for Fos were clustered in areas previously reported as active in response to these odors. In piriform cortex, activation in layers II/III shared some features with that seen in the adult; in APC, rostro-caudally oriented bands of Fos-positive cells alternated with bands relatively free of label, while labeled cells were found dispersed throughout PPC. However, in P3-P7 animals, Fos-positive cells in APC were found in a central rostro-caudally oriented band that was flanked by two bands relatively free of Fos-positive cells. This contrasted with the adult pattern, a central cell-poor band flanked by cell-rich bands, which was observed beginning at P10. These results suggest that subregions of APC visualized by odor-evoked Fos expression are active and functionally distinct shortly after birth. Changes in activity within these subregions during early postnatal development coincide with a shift toward adult-like olfactory learning behavior in the second postnatal week, and may play a role in this behavioral shift.

Immunocytochemical analysis of basket cells in rat piriform cortex.

Basket cells, defined by axons that preferentially contact cell bodies, were studied in rat piriform (olfactory) cortex with antisera to gamma-aminobutyric acid (GABA)ergic markers (GABA, glutamate decarboxylase) and to peptides and calcium binding proteins that are expressed by basket cells. Detailed visualization of dendritic and axonal arbors was obtained by silver-gold enhancement of staining for vasoactive intestinal peptide (VIP), cholecystokinin (CCK), parvalbumin, and calbindin. Neuronal features were placed into five categories: soma-dendritic and axonal morphologies, laminar distributions of dendritic and axonal processes, and molecular phenotype. Although comparatively few forms were distinguished within each category, a highly varied co-expression of features from different categories produced a "combinatorial explosion" in the characteristics of individual neurons. Findings of particular functional interest include: dendritic distributions suggesting that somatic inhibition is mediated by feedforward as well as feedback pathways, axonal variations suggesting a differential shaping of the temporal aspects of somatic inhibition from different basket cells, evidence that different principal cell populations receive input from different combinations of basket cells, and a close association between axonal morphology and molecular phenotype. A finding of practical importance is that light microscopic measurements of boutons were diagnostic for the molecular phenotype and certain morphological attributes of basket cells. It is argued that the diversity in basket cell form in the piriform cortex, as in other areas of the cerebral cortex, reflects requirements for large numbers of specifically tailored inhibitory processes for optimal operation that cannot be met by a small number of rigidly defined neuronal populations.

Functional plasticity in extrastriate visual cortex following neonatal visual cortex damage and monocular enucleation.

Neonatal lesions of primary visual cortex (areas 17, 18 and 19; VC) in cats lead to significant changes in the organization of visual pathways, including severe retrograde degeneration of retinal ganglion cells of the X/beta class. Cells in posteromedial lateral suprasylvian (PMLS) cortex display plasticity in that they develop normal receptive-field properties despite these changes, but they do not acquire the response properties of striate neurons that were damaged (e.g., high spatial-frequency tuning, low contrast threshold). One possibility is that the loss of X-pathway information, which is thought to underlie striate cortical properties in normal animals, precludes the acquisition of these responses by cells in remaining brain areas following neonatal VC damage. Previously, we have shown that monocular enucleation at the time of VC lesion prevents the X-/beta-cell loss in the remaining eye. The purpose of the present study was to determine whether this sparing of retinal X-cells leads to the development of striate-like response properties in PMLS cortex. We recorded the responses of PMLS neurons to visual stimuli to assess spatial-frequency tuning, spatial resolution, and contrast threshold. Results indicated that some PMLS cells in animals with a neonatal VC lesion and monocular enucleation displayed a preference for higher spatial frequencies, had higher spatial resolution, and had lower contrast thresholds than PMLS cells in cats with VC lesion alone. Taken together, these results suggest that preserving X-pathway input during this critical period leads to the addition of some X-like properties to PMLS visual responses.

Monocular enucleation prevents retinal ganglion-cell loss following neonatal visual cortex damage in cats.

Damage to primary visual cortex (VC) in young cats leads to severe retrograde degeneration of the dorsal lateral geniculate nucleus (dLGN) and selective transneuronal retrograde degeneration of a class of retinal ganglion cells (RGCs) that have a medium-size soma. Previous studies have shown that "programmed" RGC death associated with normal development in one eye can be attenuated by removal of the other eye, suggesting that binocular interactions can influence developmental RGC death. The present study investigated whether removal of one eye also attenuates the ganglion cell loss that accompanies an early VC lesion. Five one-week-old cats received a unilateral VC lesion (areas 17, 18, and 19), and three of these cats also underwent monocular enucleation at the same time. Two normal control animals also were examined. RGC measurements were made from flat-mounted retinae when the animals were 5 weeks old. Sampling was restricted to a retinal area corresponding to the retinotopic representation included in the VC lesion. Results indicate that there is a marked loss of medium-size RGCs in the hemiretinae projecting to the damaged hemisphere in cats that received a VC lesion alone. However, there is no such loss in VC-lesion animals that also have a monocular enucleation. These results indicate that the transneuronal RGC loss that occurs after an early visual cortex lesion can be influenced by binocular interactions.

New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that "primary" olfactory cortex functions like "association" cortex in other sensory systems.

Associational connections of pyramidal cells in rat posterior piriform cortex were studied by direct visualization of axons stained by intracellular injection in vivo. The results revealed that individual cells have widespread axonal arbors that extend over nearly the full length of the cerebral hemisphere. Within piriform cortex these arbors are highly distributed with no regularly arranged patchy concentrations like those associated with the columnar organization in other primary sensory areas (i.e., where periodically arranged sets of cells have common response properties, inputs, and outputs). A lack of columnar organization was also indicated by a marked disparity in the intrinsic projection patterns of neighboring injected cells. Analysis of axonal branching patterns, bouton distributions, and dendritic arbors suggested that each pyramidal cell makes a small number of synaptic contacts on a large number (>1000) of other cells in piriform cortex at disparate locations. Axons from individual pyramidal cells also arborize extensively within many neighboring cortical areas, most of which send strong projections back to piriform cortex. These include areas involved in high-order functions in prefrontal, amygdaloid, entorhinal, and perirhinal cortex, to which there are few projections from other primary sensory areas. Our results suggest that piriform cortex performs correlative functions analogous to those in association areas of neocortex rather than those typical of primary sensory areas with which it has been traditionally classed. Findings from other studies suggest that the olfactory bulb subserves functions performed by primary areas in other sensory systems.