Effects of Sensory and Motor Experience

There is an extensive literature showing that the structure of cortical neurons is influenced by various types of sensory and motor experience (for a review, see Kolb and Whishaw, 1998). For example, if laboratory animals ranging from rats to cats and monkeys are placed in complex environments versus living in standard lab cages, there are large changes in dendritic length and synapse number throughout the primary visual and somatosensory cortex (e.g. Greenough et al., 1985; Beaulieu and Colonnier, 1987). Similarly, if rats are trained on neuropsychological learning tasks such as a visual maze or a skilled motor learning task, then there are changes in cells in occipital cortex and motor cortex respectively (Greenough and Chang, 1988). These changes are specific, however, as visual training does not influence motor cortex neurons and visa versa.

Curiously, examination of the prelimbic region (Zilles' Cg3) of the mPFC and nearby parietal region (Par 1) in animals that were placed in complex environments for 4 months in adulthood showed an unexpected result: whereas the parietal cortex showed a large (10%) increase in dendritic length in response to this experience, there was no obvious change in the dendritic length ofthe neurons in Cg3 (Kolb et al., 2003b). This contrasting effect was especially surprising given that we have found this experience to increase dendritic length throughout the sensory and motor cortices, striatum, and nucleus accumbens. There is clearly something different about the effect of

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Figure 2: A Golgi-stained neuron in the mPFC of the rat.

Figure 2: A Golgi-stained neuron in the mPFC of the rat.

experience on the neurons in the PFC versus other regions in the forebrain. We next examined the effect of the experience on spine density, expecting that there would be no change in the Cg3 cells, but again we were mistaken: the cells showed an increase in spine density that was as large as we had seen in other cortical regions. These changes in spine density were intriguing for at least two reasons. First, this was the first time that we had observed changes in spine density in the absence of a change in dendritic length.

Second, we had previously shown that changes in spine density in response to experience are age-dependent. That is, whereas animals placed in complex environments in adulthood or senescence show significant increases in spine density in parietal and occipital cortex, animals placed in similar environments as juveniles show a significant decrease in spine density (Kolb et al., 2003a). When we looked at spine density in Cg3 of mPFC in juvenile rats, we were surprised to find that there was an increase in spine density, a result that was opposite to what we had found in sensory cortex (Fig. 3).

The failure to find parallel effects of experience on prefrontal and other cortical pyramidal cells leads to the question of whether training animals in neuropsychological tasks, which are known to be sensitive to prefrontal injuries, would produce changes similar to those observed in motor or occipital cortex of animals that have been trained in motor or visual tasks respectively. We are unaware of any systematic study of this possibility, but in an unpublished study of rats trained in a radial arm maze, a task that is sensitive to medial frontal cortex lesions in rats, we found no evidence of

Changes in Spine Density in Juveniles

Figure 3: The effects of complex housing on spine density in the parietal and prefrontal cortex of juvenile rats. There is a decrease in spine density in the parietal cortex that contrasts with an increase in spine density in the mPFC.

Parietal Frontal

Figure 3: The effects of complex housing on spine density in the parietal and prefrontal cortex of juvenile rats. There is a decrease in spine density in the parietal cortex that contrasts with an increase in spine density in the mPFC.

changes in dendritic length in mPFC (B. Kolb and G. Winocur, unpublished data). This study needs replication and extension to other neuropsychological tests, but it does suggest that once again the PFC responds differently to experience than other cortical regions. Furthermore, although the firing properties of cells in the OFC have been shown to change with the development of olfactory memories (Ramus and Eichenbaum, 2000; Schoenbaum et al., 2000; Alvarez and Eichenbaum, 2002), we are unaware of any morphological studies showing synaptic changes, and this is clearly an obvious topic for study.

The simplest conclusion from the complex housing and learning results is that placing animals in complex environments for several months or training animals to criterion in neuropsychological tests does not engage prefrontal neurons the same way that it engages sensory or motor cortical neurons. It is quite possible that the PFC is engaged only until behavioral strategies are developed, after which time it is no longer necessary, an idea that was proposed first by Hebb (1949). In contrast, sensory and motor areas are engaged as long as animals are displaying particular behaviors. The question, however, is whether there is evidence that the prefrontal cells ever change their synaptic organization or if they are simply engaging a relatively unplastic system to generate behavioral strategies. Hebb proposed that during development the PFC was especially important because it was during this time that the frontal lobe was developing schemas to solve problems that would be encountered later in life (Hebb, 1949). If this hypothesis is correct, it may be that the prefrontal cells are particularly responsive to experience during development but less so in adulthood.

Other forms of environmental stimulation do appear to produce changes in prefrontal neurons, however. For example, animals given chronic injections of corticosterone, which presumably mimics the effects of stress, show a change in organization of dendritic morphology in mPFC (Wellman, 2001). Similarly, animals given daily injections of saline, which again was presumed to be stressful, showed increased spine density in mPFC neurons (Seib and Wellman, 2003).

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