The pathways connecting the hippocampal formation, the thalamic reuniens nucleus and the thalamic reticular nucleus in the rat

Abstract

Most dorsal thalamic nuclei send axons to specific areas of the neocortex and to specific sectors of the thalamic reticular nucleus; the neocortex then sends reciprocal connections back to the same thalamic nucleus, directly as well indirectly through a relay in the thalamic reticular nucleus. This can be regarded as a 'canonical' circuit of the sensory thalamus. For the pathways that link the thalamus and the hippocampal formation, only a few comparable connections have been described. The reuniens nucleus of the thalamus sends some of its major cortical efferents to the hippocampal formation. The present study shows that cells of the hippocampal formation as well as cells in the reuniens nucleus are retrogradely labelled following injections of horseradish peroxidase or fluoro-gold into the rostral part of the thalamic reticular nucleus in the rat. Within the hippocampal formation, labelled neurons were localized in the subiculum, predominantly on the ipsilateral side, with fewer neurons labelled contralaterally. Labelled neurons were seen in the hippocampal formation and nucleus reuniens only after injections made in the rostral thalamic reticular nucleus (1.6-1.8 mm caudal to bregma). In addition, the present study confirmed the presence of afferent connections to the rostral thalamic reticular nucleus from cortical (cingulate, orbital and infralimbic, retrosplenial and frontal), midline thalamic (paraventricular, anteromedial, centromedial and mediodorsal thalamic nuclei) and brainstem structures (substantia nigra pars reticularis, ventral tegmental area, periaqueductal grey, superior vestibular and pontine reticular nuclei). These results demonstrate a potential for the thalamo-hippocampal circuitry to influence the functional roles of the thalamic reticular nucleus, and show that thalamo-hippocampal connections resemble the circuitry that links the sensory thalamus and neocortex.

Fig. 1

Photomicrograph and schematic drawing of a coronal section (bregma –1.80 mm) of the brain with a high-power view of the injection site into the TRN in the rat. VA, ventral anterior thalamic nucleus; ic, internal capsule; TRN, thalamic reticular nucleus.

Fig. 2

Photomicrograph showing numerous ipsilateral (a) and scarce contralateral (b) HRP-labelled neurons within the subiculum subsequent to HRP injections into TRN 1.8 mm caudal to bregma.

Fig. 3

Photomicrograph showing numerous ipsilateral (a) and scarce contralateral (b) FG-labelled neurons within the subiculum subsequent to FG injections into TRN 1.8 mm caudal to bregma.

Fig. 4

Photomicrograph showing labelled cells in the reuniens nucleus of the thalamus subsequent to FG injections into the rostral TRN.

Fig. 5

The number of labelled neurons per section on the ipsilateral and contralateral subicular cortex, subsequent to HRP and FG injections into the rostral TRN. The error bars on the graph give the SE, which was calculated from the average numbers of HRP- and FG-labelled neurons for each animal.

Fig. 6

Photomicrograph of one of the most important afferent connections of the rostral TRN is from layer V of the cingulate cortex.

Fig. 7

Schematic illustration of the ipsilateral pathways between hippocampal formation, TRN and the reuniens nucleus. Solid line indicates the known connections; dotted line indicates the unknown collateral connections of the hippocampal–reuniens and reuniens–hippocampal formation connections (see text). 1. Reuniens–hippocampal formation connections (Herkenham, 1978; Yanagihara et al. 1987; Su and Bentivoglio, 1990; Wouterlood et al. 1990; Dolleman-van der Weel et al. 1996, 1997; Bertram and Zhang, 1999; Dolleman-van der Weel and Witter, 2000; Vertes et al. 2007). 2. Hippocampal formation–reuniens (Aggleton et al. 1986). 3. Hippocampal formation–TRN (present study). 4. TRN–reuniens (Mckenna and Vertes, 2004). 5. Reuniens–TRN (Cornwall et al. 1990; Vertes et al. 2006; present study).