Parvalbumin and calbindin expression in parallel thalamocortical pathways in a gleaning bat, Antrozous pallidus

Abstract

The pallid bat (Antrozous pallidus) listens to prey-generated noise to localize and hunt terrestrial prey while reserving echolocation to avoid obstacles. The thalamocortical connections in the pallid bat are organized as parallel pathways that may serve echolocation and prey localization behaviors. Thalamic inputs to the cortical echolocation call- and noise-selective regions originate primarily in the suprageniculate nucleus (SG) and ventral division of medial geniculate body (MGBv), respectively. Here we examined the distribution of Parvalbumin (PV) and Calbindin (CB) expression in cortical regions and thalamic nuclei of these pathways. Electrophysiology was used to identify cortical regions selective for echolocation calls and noise. Immunohistochemistry was used to stain for PV and CB in the auditory cortex and MGB. A higher percentage (relative to Nissl-stained cells) of PV+ cells compared to CB+ cells was found in both echolocation call- and noise-selective regions. This was due to differences in cortical layers V-VI, but not layers I-IV. In the MGB, CB+ cells were present across all divisions of the MGB with a higher percentage in the MGBv than the SG. Perhaps the most surprising result was the virtual absence of PV staining in the MGBv. PV staining was present only in the SG. Even in the SG, the staining was mostly diffuse in the neuropil. These data are supportive of the notion that calcium binding proteins are differentially distributed in different processing streams. Our comparative data, however, do not support a general mammalian pattern of PV/CB staining that distinguishes lemniscal and non-lemniscal pathways.

Laminar Organization of FM Direction Selectivity in the Primary Auditory Cortex of the Free-Tailed Bat

“…Borders of layer III were between depths with decreased cell density from layer II to the localization of calretinin-positive (CR) interneurons primarily in layer IV (Figure 1E). We observed parvalbumin-positive (PV) interneurons localized in layers II–V (Figure 1F), which is consistent with findings in A1 of other species (Martin del Campo et al, 2012, 2014). Somatostatin-positive (SS) interneurons localized primarily in deep layer VI (Figure 1G).…”

“…Our estimation of the border of the cortical layer coincided with that proposed for the mouse and the Pallid bat, Antrozous pallidus (Martin del Campo et al, 2012, 2014; Nguyen et al, 2017). PV cells in the mouse auditory cortex (AC) and the pallid bat A1 extends through layer V. These authors reported that that layer V was generally distinguishable from layer IV by having larger, less dense pyramidal cells than layer IV, and thus borders could be loosely estimated based on lower cell density estimates from Nissl stain measurements (Martin del Campo et al, 2012, 2014). Cortical depth of layer IV in the free-tailed bat matches the location of this layer in the mouse and the pallid bat, where it has been described to be at 50% of the cortical depth.…”

“…The low cell-body density of layer I was in sharp contrast with the high cell density of layer II in the Nissl-stained slides (Figure 1D). Borders between layers III–V could not easily be inferred from Nissl-stained cell counts, as noted previously (Anderson et al, 2009; Martin del Campo et al, 2012, 2014). When combined with antibody labeling of inhibitory interneurons, we were able to determine borders for layer III and IV.…”

Where Do Core Thalamocortical Axons Terminate in Mammalian Neocortex When There Is No Cytoarchitecturally Distinct Layer 4?

“…To reveal neurons expressing PV, we used the PV28 anti‐PV rabbit polyclonal antibody from Swant (PV28, Swant; RRID AB_10000343) at a dilution of 1:5000. The pattern of immunoreactivity in the cerebral cortex was mostly similar across mammals, with PV being expressed in a subset of cortical neurons and their axonal projections (del Campo, Measor, and Razak 2014; Griffen and Maffei 2014; Jones 1998, 2001, 2003; Rubio‐Garrido, Perez‐De‐Manzo, and Clasca 2007).…”

Functional segregation of monaural and binaural selectivity in the pallid bat auditory cortex

“…Programmable attenuators (PA5, Tucker-Davis Technologies, Florida) allowed control of sound intensities before amplification by a stereo power amplifier (Yamaha AX430). Extracellular single-unit recordings were obtained using glass electrodes (1M NaCl, 2-10 MΩ impedance) at depths between 200 and 600 µm (layers III-V in pallid bat, Martin del Campo et al, 2014). Penetrationswere made orthogonal to the surface of the cortex.…”