Lemniscal and non‐lemniscal synaptic transmission in rat auditory thalamus.

Abstract

1. The central auditory pathway linking the inferior colliculus (IC) and the medial geniculate body (MGB) of the thalamus consists of a segregated ventral lemniscal and dorsal non-lemniscal projection whose synaptic transmission mechanisms remain unknown. Extracellular and intracellular recordings combined with axonal tract tracing and cell staining were made from lemniscal and non-lemniscal divisions of adult rat MGB maintained acutely in in vitro explants containing parallel tectothalamic projections. 2. Biocytin deposition within the brachium of the IC revealed dense axonal fibres projecting to the MGB. Thin axonal terminals were found throughout the ventral (MGv) and dorsal (MGd) divisions of the MGB. Bushy cells with tufted or bitufted dendritic branches were primarily found in the MGv. In the MGd, cells were mainly seen as stellate neurones having a radiate dendritic arbor. 3. Electrical stimulation of the brachium of IC invariably elicits fast, excitatory synaptic potentials in both MGv and MGd cells. The evoked responses occurred monosynaptically and were exclusively mediated by glutamate acting on both N-methyl-D-aspartate (NMDA) and non-NMDA receptors. Non-lemniscal MGd neurones recorded extracellularly exhibited a strong tendency to discharge in bursts in response to brachium stimulation. In contrast, a large proportion of ventral lemniscal cells tended to discharge in single or dual spikes. Intracellularly, MGd cells, but not MGv cells, showed a predominant, slow synaptic potential mediated by NMDA receptors. 4. It is concluded that the central auditory circuitry linking the tectum and the thalamus is connected monosynaptically via glutamatergic synapses. Lemniscal and non-lemniscal thalamic neurones possess distinct response properties which cannot be accounted for by a differential transmitter system or polysynaptic delays as postulated previously.

Topography and physiology of ascending streams in the auditory tectothalamic pathway

“…As such, these neurons may be more comparable to the large population of mixed inputs that has been described previously (12). Thus, the basic classes of inputs appear to be consistent with previous studies, and the few differences may reflect methodological issues, that is, photostimulation of the IC (present results) and electrical stimulation of the brachium of the IC (12,24), sampling methodology, or potential species-specific distinctions. In addition, our results extend these previous results by topographically identifying the IC sources of these excitatory and inhibitory inputs to the MGB.…”

“…Each feature by itself is not definitive; however, when used together, they helped to reconstruct nuclear location. Nevertheless, the present parcellation should be considered valid insofar as the observed topography and physiology of both the tectothalamic streams follow a pattern that is compatible with previous anatomical and physiological studies (1,11,24).…”

“…In this respect, inhibitory inputs originating from the ICl were often found to be stronger than those originating from the ICc, suggesting that MGBd neurons may be hyperpolarized preferentially and prone to low-threshold calcium spiking. Although we found no significant difference in resting potentials in vitro, the situation in vivo may differ, and previous studies suggest that MGBd neurons may rest at more hyperpolarized potentials than MGBv neurons (21,24). Similar to the excitatory inputs, the inhibitory inputs exhibited a similar level of anisotropy compared with the excitatory inputs and also were separated topographically by a greater degree than predicted.…”

“…Despite the lack of intact structures innervating the MGB in these earlier preparations, the parallel organization of the tectothalamic pathways allowed some specificity of responses from fiber stimulation (12,24). For example, Hu et al (24) demonstrated that brachial stimulation resulted in burst firing from MGBd neurons predominantly, and Bartlett and Smith (11,12) demonstrated differential excitatory and inhibitory responses to brachial stimulation in MGBv and MGBd neurons. Our preparation now enables the unambiguous localization of the tectal sources of input to the MGB, which we employed to map inputs topographically using photostimulation and to target IC regions specifically for electrical stimulation, as discussed below.…”

“…Previous investigations of the auditory tectothalamic pathways used preparations that only preserved the afferent fibers (e.g., brachium of the IC, corticothalamic fibers) to the MGB (9,11,13,24). Despite the lack of intact structures innervating the MGB in these earlier preparations, the parallel organization of the tectothalamic pathways allowed some specificity of responses from fiber stimulation (12,24).…”