Abstract
Damage involving the anterior thalamic and adjacent rostral thalamic nuclei may result in a severe anterograde amnesia, similar to the amnesia resulting from damage to the hippocampal formation. Little is known, however, about the information represented in these nuclei. To redress this deficit, we recorded units in three rostral thalamic nuclei in freely-moving rats [the parataenial nucleus (PT), the anteromedial nucleus (AM) and nucleus reuniens NRe]. We found units in these nuclei possessing previously unsuspected spatial properties. The various cell types show clear similarities to place cells, head direction cells, and perimeter/border cells described in hippocampal and parahippocampal regions. Based on their connectivity, it had been predicted that the anterior thalamic nuclei process information with high spatial and temporal resolution while the midline nuclei have more diffuse roles in attention and arousal. Our current findings strongly support the first prediction but directly challenge or substantially moderate the second prediction. The rostral thalamic spatial cells described here may reflect direct hippocampal/parahippocampal inputs, a striking finding of itself, given the relative lack of place cells in other sites receiving direct hippocampal formation inputs. Alternatively, they may provide elemental thalamic spatial inputs to assist hippocampal spatial computations. Finally, they could represent a parallel spatial system in the brain.
Highlights
The anterior thalamic nuclei appear vital for human episodic memory (Aggleton and Brown, 1999; Harding et al, 2000; Carlesimo et al, 2011), while these same thalamic nuclei in rodents are required for spatial learning (Byatt and Dalrymple-Alford, 1996; Aggleton and Nelson, 2015)
While sites within the rostral medial thalamus are vital for human episodic memory, it has proved difficult to identify the most critical nuclei and their respective contributions
Electrophysiological information concerning the AM, along with the adjacent PT and nucleus reuniens (NRe), remains exceptionally scarce even though such information may help explain the potential significance of these thalamic relays for memory
Summary
The anterior thalamic nuclei appear vital for human episodic memory (Aggleton and Brown, 1999; Harding et al, 2000; Carlesimo et al, 2011), while these same thalamic nuclei in rodents are required for spatial learning (Byatt and Dalrymple-Alford, 1996; Aggleton and Nelson, 2015). There is, a longstanding need to determine the class of information processing performed by the anterior and adjacent rostral thalamic nuclei, and why it is necessary for structures such as the hippocampus (Sutherland and Rodriguez, 1989; Aggleton et al, 2010). To address these questions, the present study examined the electrophysiological properties of rostral thalamic cells in awake, behaving rats. Lesions of the anterior thalamic nuclei that spare the anteromedial nucleus produce only partial deficits on tests of spatial learning (Aggleton et al, 1996; Byatt and Dalrymple-Alford, 1996; Van Groen et al, 2002; Peckford et al, 2014), suggesting additional contributions from the AM (Aggleton et al, 2010)
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