skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Friday, July 12 until 2:00 AM ET on Saturday, July 13 due to maintenance. We apologize for the inconvenience.


This content will become publicly available on August 8, 2024

Title: Topography of inputs into the hippocampal formation of a food‐caching bird
Abstract

The mammalian hippocampal formation (HF) is organized into domains associated with different functions. These differences are driven in part by the pattern of input along the hippocampal long axis, such as visual input to the septal hippocampus and amygdalar input to the temporal hippocampus. HF is also organized along the transverse axis, with different patterns of neural activity in the hippocampus and the entorhinal cortex. In some birds, a similar organization has been observed along both of these axes. However, it is not known what role inputs play in this organization. We used retrograde tracing to map inputs into HF of a food‐caching bird, the black‐capped chickadee. We first compared two locations along the transverse axis: the hippocampus and the dorsolateral hippocampal area (DL), which is analogous to the entorhinal cortex. We found that pallial regions predominantly targeted DL, while some subcortical regions like the lateral hypothalamus (LHy) preferentially targeted the hippocampus. We then examined the hippocampal long axis and found that almost all inputs were topographic along this direction. For example, the anterior hippocampus was preferentially innervated by thalamic regions, while the posterior hippocampus received more amygdalar input. Some of the topographies we found bear a resemblance to those described in the mammalian brain, revealing a remarkable anatomical similarity of phylogenetically distant animals. More generally, our work establishes the pattern of inputs to HF in chickadees. Some of these patterns may be unique to chickadees, laying the groundwork for studying the anatomical basis of these birds’ exceptional hippocampal memory.

 
more » « less
NSF-PAR ID:
10439961
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Journal of Comparative Neurology
Volume:
531
Issue:
16
ISSN:
0021-9967
Page Range / eLocation ID:
p. 1669-1688
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. The entorhinal cortex (EC) is the primary site of interactions between the neocortex and hippocampus. Studies in rodents and nonhuman primates suggest that EC can be divided into subregions that connect differentially with perirhinal cortex (PRC) vs parahippocampal cortex (PHC) and with hippocampal subfields along the proximo-distal axis. Here, we used high-resolution functional magnetic resonance imaging at 7 Tesla to identify functional subdivisions of the human EC. In two independent datasets, PRC showed preferential intrinsic functional connectivity with anterior-lateral EC and PHC with posterior-medial EC. These EC subregions, in turn, exhibited differential connectivity with proximal and distal subiculum. In contrast, connectivity of PRC and PHC with subiculum followed not only a proximal-distal but also an anterior-posterior gradient. Our data provide the first evidence that the human EC can be divided into functional subdivisions whose functional connectivity closely parallels the known anatomical connectivity patterns of the rodent and nonhuman primate EC.

     
    more » « less
  2. The hippocampus consists of a stereotyped neuronal circuit repeated along the septal-temporal axis. This transverse circuit contains distinct subfields with stereotyped connectivity that support crucial cognitive processes, including episodic and spatial memory. However, comprehensive measurements across the transverse hippocampal circuit in vivo are intractable with existing techniques. Here, we developed an approach for two-photon imaging of the transverse hippocampal plane in awake mice via implanted glass microperiscopes, allowing optical access to the major hippocampal subfields and to the dendritic arbor of pyramidal neurons. Using this approach, we tracked dendritic morphological dynamics on CA1 apical dendrites and characterized spine turnover. We then used calcium imaging to quantify the prevalence of place and speed cells across subfields. Finally, we measured the anatomical distribution of spatial information, finding a non-uniform distribution of spatial selectivity along the DG-to-CA1 axis. This approach extends the existing toolbox for structural and functional measurements of hippocampal circuitry. 
    more » « less
  3. Grid, place, and border cells in the mammalian hippocampus and entorhinal cortex perform highly sophisticated navigational tasks with an extremely low power budget. While previous algorithms for simultaneous localization and mapping (SLAM) in robotics have used these cells for inspiration, they have sacrificed the robust, low-power gains achieved with bioplausible models for ease of implementation. This paper presents steps towards robotic navigation with biologically realistic hippocampal models by implementing velocity-controlled oscillators, a basis for any spatially-tuned neuron, on mixed-mode neuromorphic spiking hardware. 
    more » « less
  4. Multimodal evidence suggests that brain regions accumulate information over timescales that vary according to anatomical hierarchy. Thus, these experimentally defined “temporal receptive windows” are longest in cortical regions that are distant from sensory input. Interestingly, spontaneous activity in these regions also plays out over relatively slow timescales (i.e., exhibits slower temporal autocorrelation decay). These findings raise the possibility that hierarchical timescales represent an intrinsic organizing principle of brain function. Here, using resting-state functional MRI, we show that the timescale of ongoing dynamics follows hierarchical spatial gradients throughout human cerebral cortex. These intrinsic timescale gradients give rise to systematic frequency differences among large-scale cortical networks and predict individual-specific features of functional connectivity. Whole-brain coverage permitted us to further investigate the large-scale organization of subcortical dynamics. We show that cortical timescale gradients are topographically mirrored in striatum, thalamus, and cerebellum. Finally, timescales in the hippocampus followed a posterior-to-anterior gradient, corresponding to the longitudinal axis of increasing representational scale. Thus, hierarchical dynamics emerge as a global organizing principle of mammalian brains.

     
    more » « less
  5. Abstract

    During NREM sleep, hippocampal sharp-wave ripple (SWR) events are thought to stabilize memory traces for long-term storage in downstream neocortical structures. Within the neocortex, a set of distributed networks organized around retrosplenial cortex (RS-network) interact preferentially with the hippocampus purportedly to consolidate those traces. Transient bouts of slow oscillations and sleep spindles in this RS-network are often observed around SWRs, suggesting that these two activities are related and that their interplay possibly contributes to memory consolidation. To investigate how SWRs interact with the RS-network and spindles, we combined cortical wide-field voltage imaging, Electrocorticography, and hippocampal LFP recordings in anesthetized and sleeping mice. Here, we show that, during SWR, “up-states” and spindles reliably co-occur in a cortical subnetwork centered around the retrosplenial cortex. Furthermore, retrosplenial transient activations and spindles predict slow gamma oscillations in CA1 during SWRs. Together, our results suggest that retrosplenial–hippocampal interaction may be a critical pathway of information exchange between the cortex and hippocampus.

     
    more » « less