Differential frequency-dependent antidromic resonance of the Schaffer collaterals and mossy fibers

Abstract

To better understand information transfer along the hippocampal pathways and its plasticity, here we studied the antidromic responses of the dentate gyrus (DG) and CA3 to activation of the mossy fibers and Schaffer collaterals, respectively, in hippocampal slices from naïve and epileptic rats. We applied trains of 600 electrical stimuli at functionally meaningful frequencies (θ, β/γ and γ). The responses of the DG to θ frequency trains underwent rapid potentiation that lasted about 400 stimuli, after which they progressively returned to control value. At β/γ and γ frequencies, however, the initial potentiation was followed by a strong frequency-dependent depression within the first 50 stimuli. In kindled animals, the initial potentiation was stronger than in control preparations and the resonant phase at θ frequency lasted longer. In contrast, CA3 responses were exponentially depressed at all frequencies, but depression was significantly less intense at θ frequency in epileptic preparations. Failure of fibers to fire action potentials could account for some of the aforementioned characteristics, but waveforms of the intracellular action potentials also changed as the field responses did, i.e., half-duration and time-to-peak increased in both structures along the stimulation trains. Noteworthy, block of glutamate and GABA ionotropic receptors prevented resonance and reduced the depression of antidromic responses to β/γ and γ stimulation recorded in the DG, but not in CA3. We show that the different behavior in the information transfer along these pathways depends on the frequency at which action potentials are generated, excitability history and anatomical features, including myelination and tortuosity. In addition, the mossy fibers are endowed with ionotropic receptors and terminal active properties conferring them their sui generis non-passive antidromic responses.

Entorhinal cortex lesions result in adenosine-sensitive high frequency oscillations in the hippocampus

“…Interestingly, contrary to what has been found in the DG of animal models of epilepsy (for a review see Jefferys et al, 2012), fast ripples did not appear in the DG but in CA3. This suggests that the low amplitude fast ripples observed in the DG in this study, could be originated in CA3 and transmitted to the DG by CA3-hilar-DG projections or antidromically by the mossy fibers (Vivar et al, 2012;Franco et al, 2015).…”

Persistent sodium current modulates axonal excitability in CA1 pyramidal neurons

“…This field response had a characteristic negative component (Fig. 1b), representing multiple synchronous antidromic action potentials (Franco et al 2015). The following positive component ( Fig.…”

“…b), representing multiple synchronous antidromic action potentials (Franco et al . ). The following positive component (Fig.…”

The ever-changing brain: Clinical implications

“…Moreover, they showed that these receptors coexist with glutamate receptors in the post-synaptic site. GABA acting on GABA A receptors modulates the excitability of the MFs (Ruiz et al, 2003;Treviñ o and Gutié rrez, 2005;Franco et al, 2015) and therefore further release of neurotransmitter (Treviñ o and Gutié rrez, 2005;Yamamoto et al, 2011). On the other hand, it is well known that GABA B receptors are present in the MF terminals and their activation with the agonist baclophen inhibits the release of GABA from the MFs (Gutié rrez, 2002).…”

“…Granule cells from control rats express VGlut but not VGAT, while GCs from epileptic rats (C 2 ) express both VGlut and VGAT mRNAs. the MFs acts to regulate further release of neurotransmitter and modulates information transfer of the MFs by acting on GABA A (Ruiz et al, 2003;Treviñ o and Gutié rrez, 2005;Franco et al, 2015;Yamamoto et al, 2011), as well as on GABA B receptors (Gutié rrez, 2002;Safiulina and Cherubini, 2009;Cabezas et al, 2012;Valente et al, 2015).…”