Nav1.1 channels in axon initial segments of bipolar cells augment input to magnocellular visual pathways in the primate retina

Teresa Puthussery, Sowmya Venkataramani, Jacqueline Gayet-Primo, Robert G. Smith, William Taylor

Research output: Contribution to journalArticle

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Abstract

In the primate visual system, the ganglion cells of the magnocellular pathway underlie motion and flicker detection and are relatively transient, while the more sustained ganglion cells of the parvocellular pathway have comparatively lower temporal resolution, but encode higher spatial frequencies. Although it is presumed that functional differences in bipolar cells contribute to the tuning of the two pathways, the properties of the relevant bipolar cells have not yet been examined in detail. Here, by making patch-clamp recordings in acute slices of macaque retina,weshow that the bipolar cells within the magnocellular pathway, but not the parvocellular pathway, exhibit voltage-gated sodium (Nav), T-type calcium (Cav), and hyperpolarization-activated, cyclic nucleotide-gated (HCN) currents, and can generate action potentials. Using immunohistochemistry in macaque and human retinae, we show that NaV1.1 is concentrated in an axon initial segment (AIS)-like region of magnocellular pathway bipolar cells, a specialization not seen in transient bipolar cells of other vertebrates. In contrast, CaV3.1 channels were localized to the somatodendritic compartment and proximal axon, but were excluded from the AIS, while HCN1 channels were concentrated in the axon terminal boutons. Simulations using a compartmental model reproduced physiological results and indicate that magnocellular pathway bipolar cells initiate spikes in the AIS. Finally, we demonstrate that NaV channels in bipolar cells augment excitatory input to parasol ganglion cells of the magnocellular pathway. Overall, the results demonstrate that selective expression of voltage-gated channels contributes to the establishment of parallel processing in the major visual pathways of the primate retina.

Original languageEnglish (US)
Pages (from-to)16045-16059
Number of pages15
JournalJournal of Neuroscience
Volume33
Issue number41
DOIs
StatePublished - 2013

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Visual Pathways
Primates
Retina
Ganglia
Macaca
Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
Axon Initial Segment
Cyclic Nucleotides
Presynaptic Terminals
Action Potentials
Axons
Vertebrates
Sodium
Immunohistochemistry
Calcium

ASJC Scopus subject areas

  • Neuroscience(all)
  • Medicine(all)

Cite this

Nav1.1 channels in axon initial segments of bipolar cells augment input to magnocellular visual pathways in the primate retina. / Puthussery, Teresa; Venkataramani, Sowmya; Gayet-Primo, Jacqueline; Smith, Robert G.; Taylor, William.

In: Journal of Neuroscience, Vol. 33, No. 41, 2013, p. 16045-16059.

Research output: Contribution to journalArticle

Puthussery, Teresa ; Venkataramani, Sowmya ; Gayet-Primo, Jacqueline ; Smith, Robert G. ; Taylor, William. / Nav1.1 channels in axon initial segments of bipolar cells augment input to magnocellular visual pathways in the primate retina. In: Journal of Neuroscience. 2013 ; Vol. 33, No. 41. pp. 16045-16059.
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