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Interneuron Connectivity in the Ferret and Mouse Dorsal Lateral Geniculate Nucleus

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Interneuron Connectivity in the Ferret and Mouse Dorsal Lateral Geniculate Nucleus Interneuron Connectivity in the Ferret and Mouse Dorsal Lateral Geniculate Nucleus NEUR 494 Honors Thesis Rose Elizabeth Meltzer Advisor: Judith A. Hirsch December, 2020 Meltzer Abstract The dorsal lateral geniculate nucleus (dLGN) of the thalamus is an early station in the visual pathway that provides the main input to primary visual cortex, yet its circuitry is not completely understood. Previous research from our laboratory has shown that ferret and mouse dLGN interneurons demonstrate different electrophysiological characteristics, with ferret inhibitory interneurons producing inhibitory postsynaptic currents (IPSCs) and murine interneurons producing excitatory postsynaptic currents (EPSCs). Based on these physiological differences, it was hypothesized that there were underlying differences in the anatomy of ferret and mouse dLGN. Specifically, ferret dLGN was expected to contain more dendrodendritic connections between interneurons in complex synaptic arrangements called triads. Two microscopy techniques, transmission electron microscopy (TEM) and serial block-face scanning electron microscopy (SBFSEM) were employed to investigate the differences in connectivity between ferret and mouse dLGN interneurons. GABA-stained ferret and mouse tissue was analyzed using TEM, and the results reflected species differences. Synaptic inputs to mouse interneurons were most commonly made by retinal ganglion cells, followed by other interneurons and presumed excitatory terminals. In ferret, the proportion of synaptic inputs from retinal ganglion cells, interneurons, and presumed excitatory terminals were approximately equal. In SBFSEM, spherical bundles of neurites called glomeruli contained a central retinal bouton surrounded by many interneuron dendritic profiles and other profiles in ferret, while in mouse there were many retinal boutons and few interneuron profiles. Ferret SBFSEM 3D reconstructions also revealed a unique type of interneuron that received no retinal input and provided output to many other interneurons. The major finding, that ferret interneurons are more highly interconnected and receive a proportionately smaller amount of retinal input than murine interneurons, indicates that the historical focus on axodendritic synapses between retinal ganglion cells and interneurons should expand to include dendrodendritic connections between interneurons. Additionally, these findings introduce a possible anatomical basis for electrophysiological differences between carnivore and murine dLGN that should be explored in future studies. 2 Meltzer Introduction According to a news article by the Allen Institute for Brain Science, two major unsolved mysteries about the brain are how neurons communicate with one another and how the brain computes (2019). For example, the computational unit of visual cortex, the minicolumn, is well- established, yet there is no such known fundamental unit of computation in visual thalamus (Mountcastle, 1978). Understanding the circuitry of the visual thalamus, and, more specifically, the synaptic organization of the dorsal lateral geniculate nucleus (dLGN), is vital to understanding vision. The dLGN is the first nucleus encountered by data flowing from retina, and therefore its manipulation of that data has effects that reverberate throughout the visual pathway. The general circuit of dLGN consists of retinal ganglion cells that travel through the optic nerve to provide excitatory input, intrinsic interneurons that provide local inhibition, and relay cells that project out of the dLGN to visual cortex (Hamos et al., 1985). Since interneurons influence the information passing through dLGN, understanding their connectivity and communication is necessary to unveil how dLGN changes retinal data. Furthermore, the basic dLGN circuit for feedforward inhibition in which retina innervates local interneurons that synapse on relay cells and each other is common to all mammals (Bickford, 2015), yet previous studies from our lab revealed differences in dLGN electrophysiology between species (described below) that suggested anatomical differences in this circuitry. It is therefore important to study the interneurons of diverse species to gain insight into the various strategies of vision employed by different animals. Local interneurons are unusual for cells in the brain in that they provide input through two types of synapses, one axodendritic and one dendrodendritic. The axodendritic connections are conventional synapses, requiring action potentials to generate an inhibitory postsynaptic current (IPSC) in target cells. By contrast, the dendrodendritic synapses are able to generate IPSCs in the absence of action potentials (Cox et al., 1998). In many species, dendrodendritic synapses in thalamus are involved in triads, complex synaptic arrangements involving three interconnected neurons. Triads are one of the most striking components of the thalamic microcircuitry and have been studied extensively. However, the literature has focused, with rare exception, on one type of triad in which a retinal bouton is presynaptic to an interneuron dendrite and a relay cell dendrite. In these arrangements the interneuron dendrite then dendrodendritically synapses on the relay 3 Meltzer cell dendrite to complete the triad (Rapisardi and Miles, 1984; Sherman, 2004; Heiberg et al., 2016). Our recordings from carnivore and recent studies suggest that interneurons are also involved in a different type of triad (or its electrotonic equivalent) consisting of one retinal ganglion cell that provides excitatory input to two inhibitory interneurons connected by a dendrodendritic synapse. In ferret and cat dLGN interneurons, visual stimuli evoke unitary IPSCs preceded by a depolarizing notch. These notches appear to be excitatory postsynaptic potentials (EPSCs) terminated by the subsequent IPSCs (Fig. 1). Since the timing of an IPSC comes quickly after a notch, it is unlikely that IPSCs are produced by traditional axodendritic synapses. Rather, quick and local dendrodendritic transmitter release seems more likely. We propose that retinal bouton-interneuron dendrite-interneuron dendrite triads (or their electrotonic equivalent (Fig. 1E)) are the structural basis for the notch-IPSC events recorded from carnivore. Interestingly, recordings from murine interneurons show EPSCs that are not truncated by IPSCs (Fig. 2). This contrast between mouse and ferret indicates underlying anatomical differences between species. Since IPSCs are generally not recorded from murine interneurons, we hypothesize that the connectivity of mouse dLGN differs from that of ferret, with mouse potentially consisting of fewer retinal bouton-interneuron-interneuron synaptic triads. 4 Meltzer 100 pA 100 pA 100 pA 100 pA Figure 1. Synaptic physiology of relay cells and interneurons in carnivores. (A) Recordings of membrane currents from cat relay cell (black) and interneuron (blue); anatomical reconstructions of the recorded cells depicted on the left. A, B adapted from Suresh, 2017. (B) Recordings from a ferret relay cell and interneuron; conventions as in A. (C) Synaptic physiology of interneurons in carnivore. Recording of membrane currents from an interneuron in the ferret dLGN is dominated by ② serial IPSCs that are usually preceded by ① small depolarizing notches. (D, E) Hypothetical wiring diagrams for C. (D) ① Two interneuronal dendritic terminals (blue) receive excitatory input from the same retinal bouton (pink), and ② one interneuron dendritic terminal synapses on the other in ferret. (E) Electrotonic equivalent of D. Two interneurons receive input from the same retinal ganglion cell at a distance from the synapse between two interneuron dendritic terminals; conventions as in D. 5 Meltzer 100 pA Figure 2. Synaptic physiology of interneurons in rodents. (A) Recording of optogenetically identified murine interneuron. (B) Synaptic physiology of interneurons in mouse. Example recording from an interneuron in the mouse dLGN is dominated by ① serial, unitary EPSCs. (C) Hypothetical wiring diagram to explain B does not require dendrodendritic inhibitory input; conventions as in Figure 1. To investigate our hypothesis that species differences in the electrophysiology of interneurons is due to underlying anatomical differences, we employed two microscopy techniques. Transmission electron microscopy (TEM) and serial block-face scanning electron microscopy (SBFSEM) were used to observe and compare the anatomy of mouse and ferret dLGN. TEM, a 2D technique, was used to quantify the retinal and interneuronal synaptic inputs to interneurons in mouse and ferret. This technique was well-suited to the task because each image covered a large area of dLGN, providing a representative population sample, and GABA staining made it possible to identify interneurons with a high degree of certainty. SBFSEM created a stack of images taken at regular intervals throughout a tissue volume, which allowed for structures like interneuron dendritic segments and retinal axon segments to be traced throughout the stack and reconstructed in 3D. These 3D reconstructions were useful in following neurite segments through the tissue and marking retinal bouton-interneuron-interneuron triads that could not have been observed in TEM since all three synapses rarely occur in one plane of section (Fig. 1D). 6 Meltzer SBFSEM would have also made it possible to observe the electrotonic equivalent of these triads, complex synaptic arrangements that occur at a distance but result in the same electrophysiological
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