Nucleus Reuniens Thalami Modulates Activity in Hippocampal Field CA1 through Excitatory and Inhibitory Mechanisms

Abstract

The nucleus reuniens thalami (RE) originates dense projections to CA1, forming asymmetrical synapses on spines (50%) and dendrites (50%). The hypothesis that RE input modulates transmission in CA1 through excitation of both pyramidal cells and interneurons was tested using electrophysiological methods in the anesthetized rat. The RE-CA1 afferents were selectively stimulated at their origin; evoked field potentials and unit activity were recorded in CA1. RE-evoked depth profiles showed a prominent negative deflection in the stratum lacunosummoleculare and a positive one in the stratum radiatum. The lacunosum-moleculare sink-radiatum source configuration is compatible with RE-elicited depolarization of apical dendrites of pyramidal cells. Despite a consistent and robust paired pulse facilitation of RE-evoked field potentials, population spikes in the stratum pyramidale were not detected at any tested condition. This indicates the inability of RE-CA1 input to discharge pyramidal cells. However, stimulation of RE-elicited spiking of extracellularly recorded units in strata oriens/alveus and distal radiatum, indicative of the activation of local interneurons. Thus, RE seems to modulate transmission in CA1 through a (subthreshold) depolarization of pyramidal cells and a suprathreshold excitation of putative inhibitory oriens /alveus and radiatum interneurons.RE-evoked monosynaptic or disynaptic field potentials were associated with stimulation of rostral or caudal RE, respectively. Anatomically, a projection from caudal to rostral RE was demonstrated that can account for the disynaptic RE-CA1 input. Because caudal RE receives input from the hippocampus via the subiculum, we propose the existence of a closed REhippocampal circuit that allows RE to modulate the activity in CA1, depending on hippocampal output. Key words: rat; electrophysiology; neuroanatomical tracing; hippocampus; midline thalamus; limbic system; learning and memoryThe involvement of thalamic midline nuclei in early stages of Alzheimer's disease Braak, 1991, 1992) and in diencephalic amnesia (Rousseau, 1994) has recently drawn attention to the connectivity between the nucleus reuniens (RE) and structures of the medial temporal lobe (Herkenham, 1978;Wouterlood et al., 1990;Dolleman-Van der Weel and Witter, 1996). In this study we focused on the RE projection to hippocampal field CA1, a crucial structure for learning and memory processes (Squire, 1992).A few investigators have studied the contribution of RE to hippocampal f unctioning. Vanderwolf et al. (1985) examined whether the medial thalamic nuclei, including RE, were involved in generating hippocampal atropine-resistant theta rhythm. Their extensive radiofrequency lesions, however, resulted in little or no effect on this type of rhythmical activity. Hirayasu and Wada (1992a,b) injected NMDA in the thalamic midline of the rat. When NMDA was administered to RE, it caused tonic and/or clonic generalized convulsions associated with temporal limbic EEG seizure discharge. They proposed that RE partic...

The hippocampus participates in a pharmacological rat model of absence seizures

“…How the hippocampal units fire 40-80 ms in advance to the thalamic negative PD is not known. It is known that thalamic inputs can excite hippocampus (CA1 and subiculum) neurons (Dolleman- Van der Weel et al, 1997;Bertram and Zhang, 1999;Vertes et al, 2007). Intrinsic resonance of hippocampal pyramidal cells at 4-10 Hz (Leung and Yu, 1998) or a decrease in inhibition (Perez Velazquez et al, 2007) may enhance the response to rhythmic excitation.…”

“…1B). The hippocampal CA1 area is known to receive afferents from the midline thalamus (Dolleman- Van der Weel et al, 1997). An electrode was glued to the anterior side of the guide cannula, and wire electrodes were also implanted into the ventrolateral thalamic nucleus bilaterally and the right frontal cortex (coordinates above).…”

Neurotoxic lesions of the thalamic reuniens or mediodorsal nucleus in rats affect non-mnemonic aspects of watermaze learning

“…Behavioural considerations in relation to thalamic-mPFC connectivity Afferents from RE were shown to exert excitatory effects on mPFC, similar to actions in the hippocampus, and thus RE appears to be in a position to influence and/or coordinate activity in both systems (Dolleman- Van der Weel et al 1997;Di Prisco and Vertes 2006). RE neurons, receiving input from mPFC, have been shown to innervate the hippocampal CA1 area.…”

Magnetic Resonance Imaging in the Study of the Lithium–Pilocarpine Model of Temporal Lobe Epilepsy in Adult Rats

“…First, the known anatomic connections of the thalamus to the limbic system and its excitatory input to these structures indicate its central role in limbic seizures. Indeed, thalamic stimulation yields short-latency excitatory responses in the entorhinal cortex and hippocampus (30)(31)(32). Moreover, in a number of studies using different models for limbic SE, the 2-deoxyglucose mapping of metabolic activity has underscored clearly the involvement of the midline thalamic nuclei (33)(34)(35)(36).…”