Organization of excitatory and inhibitory local networks in the caudal nucleus of tractus solitarius of rats revealed in in vitro slice preparation

Abstract

Morphological and physiological properties of neurons in the caudal nucleus of tractus solitarius (NTS) of rats were studied in vitro by whole-cell recording and intracellular staining with biocytin. Synaptic responses following the solitary tract stimulation were also investigated to elucidate anatomical substrates of the underlying local circuits. Biocytin-filled NTS cells were divided into three groups according to the pattern of their axonal arborization: (1) local circuit neurons whose axon collaterals were extensively distributed within the NTS with the main axons leaving the NTS; (2) presumed interneurons whose axon collaterals seemed to be restricted within the NTS; and (3) projection neurons whose axons had few, if any, collaterals. Both local circuit neurons and presumed interneurons had small cell bodies (< 150 microns2 in somal area) and exhibited tonic regular spiking at depolarized membrane potentials. Polysynaptic excitatory background activity was increased and lasted for 300-1000 msec in these neurons following solitary tract stimulation. The projection neurons had medium to large cell bodies (> 150 microns2 in somal area). Inhibitory postsynaptic responses produced by an increased CI-conductance were recorded in these projection neurons. These findings suggest that excitatory local networks are organized by an assembly of the local circuit neurons in the caudal NTS, and that the interneurons are arranged to connect the excitatory local network with medium to large projection neurons via inhibitory synapses. Visceral afferent information is probably processed in the highly organized excitatory and inhibitory local networks within the caudal NTS and conveyed to other brain regions.

Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat

“…Our data confirm neurophysiologically the previously published anatomical observations showing that the TS terminals make monosynaptic asymmetric contact with the dendrites of viscerally projecting DMX neurons in the cNTS regions [11,21,25]. Such a monosynaptic vago-vagal connection has also been functionally suggested by the authors of studies using slice preparations of rats and guinea pigs [16,22,24]. The novel finding of the present study is that, unlike the TS-NTS synapses that consistently exhibit strong short-term depression [13,26,36,37] and this study, the TS-DMX synapses show distinct types of short-term plasticity ranging from paired-pulse depression to facilitation, which results primarily from the distinct release properties of each afferent fiber.…”

“…In particular, we compared the frequency dependence between the well-studied NTS neurons [7,13,16-20] and the much less studied DMX neurons [10,11,16,21-24] that also form a part of vago-vagal reflex pathway [25]. Our findings show that distinct classes of postsynaptic neurons show distinct types of short-term plasticity and frequency dependence resulting from distinct presynaptic mechanisms, depending on the type and function of each neuron.…”

Characterization of neurons of the nucleus tractus solitarius pars centralis

“…Some membrane properties of cNTS neurons, however, seem to indicate that these neurons have characteristics that distinguish them from other NTS neurons, most noticeably the smaller soma area and the higher input resistance [12,14,17,19,26,32,34]. These electrophysiological membrane features would seem to be best suited to signaling the fast dynamic changes in esophageal pressure observed during the passage of a bolus in the esophagus, since even minute changes in neurotransmitter release would induce large changes in the membrane potential.…”

“…Various groups have reported recently that NTS neurons display a certain degree of morphological and electrophysiological diversity [12,14,[18][19][20]26,34]. These observations suggest that it may be possible to differentiate between neurons subserving similar functions from adjacent neurons devoted to different roles.…”

“…A vast array of studies have shown that sensory vagal information to NTS neurons is excitatory and uses, principally, excitatory amino acids such as glutamate [3,[14][15][16][17]21,23,29,33]. Lu and Bieger recently reported that glutamate was the neurotransmitter mediating fast excitatory neurotransmission from vagal afferent fibers to cNTS neurons [23]; however, they did not characterize the glutamatergic receptors subtype(s) involved.…”