Hyperpolarization-activated currents in isolates superior colliculus-projecting neurons from rat visual cortex

Joel Solomon, J. M. Nerbonne

Research output: Contribution to journalArticle

38 Citations (Scopus)

Abstract

In vivo injections of rhodamine beads into the superior colliculus of 4-9 postnatal day rat pups label a population of layer 5 cells in the primary visual cortex that can be identified in tissue sections or dissociated cell cultures. Under voltage clamp, hyperpolarizations of isolated superior colliculus-projecting (SCP) neurons from rest elicit an instantaneous inward current (I(inst)) with nearly linear current-voltage properties that is not blocked by extracellular application of 3 mM CsCl. Voltage clamp steps to potentials more negative than -60 mV evoke a slowly activating, non-inactivating inward current that is not blocked by 1 μM TTX, 1 mM 4-aminopyridine (4-AP), 5 mM Co2+, or 25 mM TEA, but is potently blocked by extracellular application of 3 mM CsCl. This current is similar to I(h) described in other systems. I(h), the time-dependent inward current in SCP neurons, begins to activate near the resting membrane potential and reaches full activation at -110 mV. The voltage dependence of activation is well fitted by a Boltzmann distribution with the membrane potential at half-maximal activation ( V 1/2 ) = -81.0 mV and s (steepness of the curve parameter) = 7.2 mV. Thus, I(h) may contribute to setting the resting membrane potential and resting input resistance of SCP neurons. The inward rectification of the whole-cell current vs. voltage relation is accounted for by the voltage dependence of I(h) activation. Current through the activated h-conductance shows slight outward rectification that is accounted for by constant field considerations. The h-conductance is substantially permeable only to sodium and potassium and, under normal physiological conditions, is expected to reverse at approximately -22 mV at 20°C. For [K+](o) ≤ 20 mM and 120 mM ≥ [Na+](o) ≥ 70 mM, I(h) obeys independence with a P(Na)/P(K) (ratio of Na+ to K+ permeability) of 0.40. Extracellular potassium increases g(h). If this effect is modelled as the result of potassium binding to an extracellular conductance-permitting site, potassium has an apparent dissociation constant (K(app)) of 25.7 mM and the ability to maximally increase g(h) in the order of 10-fold over basal levels. I(h) underlies the depolarizing 'sag' and 'overshoot' observed in SCP neurons following the onset and offset, respectively, of hyperpolarizing current injections. In addition, I(h) appears to control the duration and the frequencv of repetitive firing following the cessation of sustained hyperpolarizing current injections. Taken together, these results suggest that I(h) plays an important role in modulating the response of SCP neurons to inhibitory and excitatory synaptic inputs.

Original languageEnglish (US)
Pages (from-to)393-420
Number of pages28
JournalJournal of Physiology
Volume462
StatePublished - 1993
Externally publishedYes

Fingerprint

Superior Colliculi
Visual Cortex
Neurons
Potassium
Membrane Potentials
Injections
4-Aminopyridine
Rhodamines
Permeability
Cell Culture Techniques
Sodium
Population

ASJC Scopus subject areas

  • Physiology

Cite this

Hyperpolarization-activated currents in isolates superior colliculus-projecting neurons from rat visual cortex. / Solomon, Joel; Nerbonne, J. M.

In: Journal of Physiology, Vol. 462, 1993, p. 393-420.

Research output: Contribution to journalArticle

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