Influence of Highly Distinctive Structural Properties on the Excitability of Pyramidal Neurons in Monkey Visual and Prefrontal Cortices

Abstract

Whole-cell patch-clamp recordings and high-resolution 3D morphometric analyses of layer 3 pyramidal neurons in in vitro slices of monkey primary visual cortex (V1) and dorsolateral granular prefrontal cortex (dlPFC) revealed that neurons in these two brain areas possess highly distinctive structural and functional properties. Area V1 pyramidal neurons are much smaller than dlPFC neurons, with significantly less extensive dendritic arbors and far fewer dendritic spines. Relative to dlPFC neurons, V1 neurons have a significantly higher input resistance, depolarized resting membrane potential and higher action potential (AP) firing rates. Most V1 neurons exhibit both phasic and regular-spiking tonic AP firing patterns, while dlPFC neurons exhibit only tonic firing. Spontaneous postsynaptic currents are lower in amplitude and have faster kinetics in V1 than in dlPFC neurons, but are no different in frequency. Three-dimensional reconstructions of V1 and dlPFC neurons were incorporated into computational models containing Hodgkin-Huxley and AMPA- and GABAA-receptor gated channels. Morphology alone largely accounted for observed passive physiological properties, but led to AP firing rates that differed more than observed empirically, and to synaptic responses that opposed empirical results. Accordingly, modeling predicts that active channel conductances differ between V1 and dlPFC neurons. The unique features of V1 and dlPFC neurons are likely fundamental determinants of area-specific network behavior. The compact electrotonic arbor and increased excitability of V1 neurons support the rapid signal integration required for early processing of visual information. The greater connectivity and dendritic complexity of dlPFC neurons likely support higher level cognitive functions including working memory and planning.

Strychnine-sensitive glycine receptors on pyramidal neurons in layers II/III of the mouse prefrontal cortex are tonically activated

“…In total, identified LII/III PNs (n ϭ 30) had a RMP of Ϫ67.9 Ϯ 1 mV, I R ϭ 156 Ϯ 9 M⍀, membrane time constant ( m ) ϭ 28 Ϯ 2 ms, membrane capacitance (C m ) ϭ 176 Ϯ 7 pF, rheobase ϭ 111 Ϯ 10 pA, and firing threshold ϭ Ϫ38 Ϯ 1 mV (Table 1), all of which are consistent with previous reports for PNs in this area (Amatrudo et al 2012;Kawaguchi 1993). When prolonged depolarizing current injections were made at RMP, the LII/III neurons fired in a pattern characteristic of PNs, including pronounced accommodation of firing rate.…”

“…1A) and confirmed to be LII/III PNs of the prelimbic region of the mPFC on the basis of morphological and electrophysiological properties. PFC PNs have specific intrinsic and firing properties that distinguish them from GABAergic interneurons, the other principal neuronal subtype within layer II/III (Amatrudo et al 2012;Kawaguchi 1993).…”

“…Additionally, sag was significantly greater in layer V/VI (sag ϭ 4.0 Ϯ 0.5, P Ͻ 0.05). It should be noted that when recorded at room temperature (Amatrudo et al 2012;Kawaguchi 1993), cortical PNs have higher I R and lower rheobase than at more physiological temperatures without effects on RMP and I h (Day et al 2005;Thuault et al 2013). For a detailed description of the effects of recording temperature on cortical PNs, see Hedrick and Waters (2012).…”

Diversity of Glutamatergic Synaptic Strength in Lateral Prefrontal versus Primary Visual Cortices in the Rhesus Monkey

“…Standard tight-seal, whole-cell patch-clamp recordings with simultaneous biocytin filling were obtained from L3 pyramidal cells as described previously (Chang et al, 2005;Amatrudo et al, 2012;. Cells were visualized under infrareddifferential interference contrast optics, and electrodes were fabricated on a horizontal Flaming and Brown micropipette puller (model P-87, Sutter Instruments).…”

“…Access resistance was monitored throughout the duration of each experiment, and signals were low-pass filtered at 10 kHz. For cell inclusion in electrophysiological analyses, cells were required to have a resting membrane potential ՅϪ55 mV, stable access resistance, an AP overshoot, and the ability to fire repetitive APs in response to prolonged depolarizing current steps, as described previously (Chang et al, 2005;Amatrudo et al, 2012;.…”