The perirhinal cortex (PER), which is critical for associative memory and stimulus discrimination, has been described as a wall of inhibition between the neocortex and hippocampus. With advanced age, rats show deficits on PER-dependent behavioral tasks and fewer PER principal neurons are activated by stimuli, but the role of PER interneurons in these altered circuit properties in old age has not been characterized. In the present study, PER neurons were recorded while rats traversed a circular track bidirectionally in which the track was either empty or contained eight novel objects evenly spaced around the track. Putative interneurons were discriminated from principal cells based on the autocorrelogram, waveform parameters, and firing rate. While object modulation of interneuron firing was observed in both young and aged rats, PER interneurons recorded from old animals had lower firing rates compared with those from young animals. This difference could not be accounted for by differences in running speed, as the firing rates of PER interneurons did not show significant velocity modulation. Finally, in the aged rats, relative to young rats, there was a significant reduction in detected excitatory and inhibitory monosynaptic connections. Together these data suggest that with advanced age there may be reduced afferent drive from excitatory cells onto interneurons that may compromise the wall of inhibition between the hippocampus and cortex. This circuit dysfunction could erode the function of temporal lobe networks and ultimately contribute to cognitive aging.

It has been proposed that as animals explore their environment they build and maintain a cognitive map, an internal representation of their surroundings (Tolman, 1948). We tested this hypothesis using a task designed to assess the ability of rats to make a spatial inference (take a novel shortcut)(Roberts et al., 2007). Our findings suggest that rats are unable to make a spontaneous spatial inference. Furthermore, they bear similarities to experiments which have been similarly unable to replicate or support Tolman’s (1948) findings. An inability to take novel shortcuts suggests that rats do not possess a cognitive map (Bennett, 1996). However, we found evidence of alternative learning strategies, such as latent learning (Tolman & Honzik, 1930b) , which suggest that rats may still be building such a representation, although it does not appear they are able to utilise this information to make complex spatial computations. Neurons found in the hippocampus show remarkable spatial modulation of their firing rate and have been suggested as a possible neural substrate for a cognitive map (O'Keefe & Nadel, 1978). However, the firing of these place cells often appears to be modulated by features of an animal’s behaviour (Ainge, Tamosiunaite, et al., 2007; Wood, Dudchenko, Robitsek, & Eichenbaum, 2000). For instance, previous experiments have demonstrated that the firing rate of place fields in the start box of some mazes are predictive of the animal’s final destination (Ainge, Tamosiunaite, et al., 2007; Ferbinteanu & Shapiro, 2003). We sought to understand whether this prospective firing is in fact related to the goal the rat is planning to navigate to or the route the rat is planning to take. Our results provide strong evidence for the latter, suggesting that rats may not be aware of the location of specific goals and may not be aware of their environment in the form of a contiguous map. However, we also found behavioural evidence that rats are aware of specific goal locations, suggesting that place cells in the hippocampus may not be responsible for this representation and that it may reside elsewhere (Hok, Chah, Save, & Poucet, 2013). Unlike their typical activity in an open field, place cells often have multiple place fields in geometrically similar areas of a multicompartment environment (Derdikman et al., 2009; Spiers et al., 2013). For example, Spiers et al. (2013) found that in an environment composed of four parallel compartments, place cells often fired similarly in multiple compartments, despite the active movement of the rat between them. We were able to replicate this phenomenon, furthermore, we were also able to show that if the compartments are arranged in a radial configuration this repetitive firing does not occur as frequently. We suggest that this place field repetition is driven by inputs from Boundary Vector Cells (BVCs) in neighbouring brain regions which are in turn greatly modulated by inputs from the head direction system. This is supported by a novel BVC model of place cell firing which predicts our observed results accurately. If place cells form the neural basis of a cognitive map one would predict spatial learning to be difficult in an environment where repetitive firing is observed frequently (Spiers et al., 2013). We tested this hypothesis by training animals on an odour discrimination task in the maze environments described above. We found that rats trained in the parallel version of the task were significantly impaired when compared to the radial version. These results support the hypothesis that place cells form the neural basis of a cognitive map; in environments where it is difficult to discriminate compartments based on the firing of place cells, rats find it similarly difficult to discriminate these compartments as shown by their behaviour. The experiments reported here are discussed in terms of a cognitive map, the likelihood that such a construct exists and the possibility that place cells form the neural basis of such a representation. Although the results of our experiments could be interpreted as evidence that animals do not possess a cognitive map, ultimately they suggest that animals do have a cognitive map and that place cells form a more than adequate substrate for this representation.

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