Projection-specific integration of convergent thalamic and retrosplenial signals in the presubicular head direction cortex

Abstract

Head-direction (HD) signals function as the brain's internal compass. They are organized as an attractor, and anchor to the environment via visual landmarks. This association might happen in the dorsal presubiculum. We find converging monosynaptic excitatory connections from anterior thalamic nucleus and from retrosplenial cortex on single layer 3 presubicular neurons. Independent dual wavelength photostimulation of these inputs in slices leads to action potential generation preferentially for near-coincident inputs, sending an integrated HD signal to medial entorhinal cortex. Layer 4 neurons send their axons to the lateral mammillary nucleus. However, their dendrites avoid overlap with thalamic and retrosplenial axons. Action potentials in layer 4 neurons may be initiated following di-synaptic excitation via layer 3, indicating that landmark updating of HD signals in the lateral mammillary nucleus is a two-step process. Thus, a coherent sense of orientation involves projection specific translaminar processing in the presubiculum.

In Memoriam: Richard Miles: Neuroscience network has lost a key synapse

“…How do excitatory and inhibitory neurons interact, and may this support head directional firing (Nassar et al, 2018;Simonnet et al, 2017)? Optogenetics let us examine converging inputs (Richevaux et al, 2023), but how do these signals stabilize or flexibly reset the attractor? More work is needed, he would say.…”