Local origin of excitatory-inhibitory tuning equivalence in a cortical network.

The interplay between excitation and inhibition determines the fidelity of cortical representations. The receptive fields of excitatory neurons are often finely tuned to encoded features, but the principles governing the tuning of inhibitory neurons remain elusive. In this study, we recorded populations of neurons in the mouse postsubiculum (PoSub), where the majority of excitatory neurons are head-direction (HD) cells. We show that the tuning of fast-spiking (FS) cells, the largest class of cortical inhibitory neurons, was broad and frequently radially symmetrical. By decomposing tuning curves using the Fourier transform, we identified an equivalence in tuning between PoSub-FS and PoSub-HD cell populations. Furthermore, recordings, optogenetic manipulations of upstream thalamic populations and computational modeling provide evidence that the tuning of PoSub-FS cells has a local origin. These findings support the notion that the equivalence of neuronal tuning between excitatory and inhibitory cell populations is an intrinsic property of local cortical networks.

Thalamocortical processing of the head-direction sense.

Our thoughts and sensations are examples of cognitive processes that emerge from the collective activity of billions of neurons in the brain. Thalamocortical circuits form the canonical building-blocks of the brain networks supporting the most complex cognitive functions. How these neurons communicate and interact has been the focus of extensive research in "classical" sensory systems. Similar to visual, auditory or somatosensory thalamic pathways, one primary nucleus in the anterior (limbic) thalamus - the antero-dorsal nucleus - conveys a low-level input, the head-direction (HD) signal, to the cortex. Its activity is controlled in large part by the vestibular system and is relayed by a serially connected group of subcortical nuclei to the thalamus. HD cells serve as the brain's internal 'compass' and each of them is tuned to the specific direction the animal is facing. Recently, recordings of HD neuronal populations in the antero-dorsal nucleus and its main cortical target, the post-subiculum, have revealed that neuronal activity in the thalamocortical HD network are largely invariant to brain states at three levels: static (preserved functional organization), temporal (same drifting speed during exploration and Rapid Eye Movement sleep) and inter-area interaction (from thalamus to cortex). These observations suggest that HD neurons are certainly more driven by intrinsic wiring and dynamics than by sensory inputs and that the information flows bottom-up, even during sleep. Altogether, thalamic HD cells convey a highly reliable, near-noiseless signal that broadly influences the emergence of spatial maps in the cortex and may play a key role in sleep-dependent memory processes.