Anatomical organization of presubicular head-direction circuits

Abstract

Neurons coding for head-direction are crucial for spatial navigation. Here we explored the cellular basis of head-direction coding in the rat dorsal presubiculum (PreS). We found that layer2 is composed of two principal cell populations (calbindin-positive and calbindin-negative neurons) which targeted the contralateral PreS and retrosplenial cortex, respectively. Layer3 pyramidal neurons projected to the medial entorhinal cortex (MEC). By juxtacellularly recording PreS neurons in awake rats during passive-rotation, we found that head-direction responses were preferentially contributed by layer3 pyramidal cells, whose long-range axons branched within layer3 of the MEC. In contrast, layer2 neurons displayed distinct spike-shapes, were not modulated by head-direction but rhythmically-entrained by theta-oscillations. Fast-spiking interneurons showed only weak directionality and theta-rhythmicity, but were significantly modulated by angular velocity. Our data thus indicate that PreS neurons differentially contribute to head-direction coding, and point to a cell-type- and layer-specific routing of directional and non-directional information to downstream cortical targets.DOI: http://dx.doi.org/10.7554/eLife.14592.001

Complementary Modular Microcircuits of the Rat Medial Entorhinal Cortex

“…Projections from presubiculum preferentially label axons in layer 3 and deep layer 1 of MEC and form thin septa in layer 2 MEC, while projections from parasubiculum terminate in relatively large clusters in MEC layer 2 (Witter et al, 1989; van Groen and Wyss, 1990). This is also supported at the single cell level by reconstructions of single axons from the presubiculum (Preston-Ferrer et al, 2016) and the parasubiculum (Burgalossi et al, 2011) to the superficial layers of the MEC. The connectivity from the presubiculum has been studied in detail by Witter and colleagues who showed that presubicular inputs target apical dendrites of layer 5 entorhinal neurons and also neurons in all other layers of entorhinal cortex (Caballero-Bleda and Witter, 1993; Wouterlood et al, 2004; Canto et al, 2012).…”

“…The presubiculum contains clusters, which are largely restricted to PrS L2, are surrounded by calbindin- positive cells ( Figure 8A ; Fujise et al, 1995; Preston-Ferrer et al, 2016). These clusters also stain for acetylcholinesterase ( Figure 8B ).…”

“…Both the pre- and parasubiculum contain a large proportion of head direction cells (Boccara et al, 2010; Tang et al, 2016) which have been proposed to play a crucial role in the generation of grid activity. Head-direction cells in both PaS (Burgalossi et al, 2011) and PrS (Preston-Ferrer et al, 2016) have been shown to project to the MEC, and they might represent two parallel sources of HD inputs to grid cell system in MEC.…”

Laminar Localization and Projection-Specific Properties of Presubicular Neurons Targeting the Lateral Mammillary Nucleus, Thalamus, or Medial Entorhinal Cortex

“…The presubicular projection may be essential for serially transferring the head direction signal from the ATN to the medial entorhinal grid cell system (Rowland et al, 2013; Preston-Ferrer et al, 2016). Other known projection targets of the PrS include feedback projections to the thalamus (van Groen and Wyss, 1990a,b; Ishizuka, 2001) and LMN (Allen and Hopkins, 1989; Gonzalo-Ruiz et al, 1992).…”

Influences of photic stress on postsubicular head‐directional processing

“…Due to the nature of our tetrode recordings, we cannot deduce with certainty the layer specificity of our recorded head‐direction cells. However, results from a recent study (Preston‐Ferrer et al ., ) showing a decreased theta rhythmicity specific to layer 3 postsubicular neurons (compared to layer 2 neurons) are consistent with our own data. Layer 3 neurons were found to predominately project to the medial entorhinal cortex, whereas layer 2 neurons targeted the retrosplenial cortex, as well as contralateral presubiculum.…”