Kindling Changes Burst Firing, Neural Synchrony and Tonotopic Organization of Cat Primary Auditory Cortex

Abstract

The effect of electrical kindling, applied twice daily in primary auditory cortex on the neural response properties and tonotopic organization in the lightly ketamine anesthetized cat is presented. Kindling refers to a highly persistent modification of brain functioning in response to repeated application of initially sub-convulsant electrical stimulation, typically in the limbic system but here in auditory cortex, which results in the development of epileptiform activity. Kindling resulted in approximately two-thirds of the animals reaching a fully generalized state in 40 stimulation sessions. Multi-unit recordings were obtained from primary auditory cortex contralateral to the kindled site. Spontaneous activity of single units in fully kindled animals showed a decrease in the mean firing rate compared to sham controls, and a reduction in the rate of burst firing as well as in the mean interspike interval in a burst as compared with normal and sham controls. A 40% enhancement of spontaneous neural synchrony, as measured by spike cross-correlation, was found. Hearing sensitivity, measured by auditory brainstem response, was not affected by the kindling sessions. A profound alteration of the tonotopic map in AI was observed with a large extent becoming tuned to similar high characteristic frequencies. The percentage of double tuned neurons was significantly increased, nevertheless the frequency-tuning curve bandwidth was on average reduced. Thus, electrical kindling resulted in substantial alterations in unit firing characteristics and reorganization of cat auditory cortex.

Cortical abnormalities in epilepsy revealed by local EEG synchrony

“…Our findings indicate that regions of locally enhanced synchronized neuronal activity exist in patients with epilepsy. These findings are consistent with earlier reports of localized synchrony measurements in human epilepsy patients (Le Van Quyen, Soss et al 2005) and a cat model of seizures (Valentine, Teskey et al 2004). LH regions appear to be stable, i.e.…”

“…In those patients in whom the epileptogenic zone was covered by the subdural grid, there appeared to be an association between the epileptogenic zone and LH regions, however they were more likely to be adjacent than concordant, as demonstrated by Patients 1, 2, 4, 6, and 8. These findings are consistent with prior observations of elevated local coherence over tumors and epileptogenic areas observed during intraoperative corticography (Towle, Syed et al;Towle, Carder et al 1999), waveletbased synchrony in chronic ICEEG recordings of a patient with a large frontal tumor (Le Van Quyen, Soss et al 2005) and cross correlation of microelectrode recordings using a non-lesional cat model of seizures (Valentine, Teskey et al 2004). In the cases in which there was concordance between the epileptogenic zone and an LH region (Patients 5, 6, and 9), the epileptogenic zone (or the portion that was recorded from the subdural grid) was determined primarily from interictal activity rather than from seizure onsets.…”

Correlated neural activity as the driving force for functional changes in auditory cortex

“…During development (Zhang et al, 2002;Nakahara et al, 2004) and also following peripheral (Rajan et al, 1993) or central ''injury'' (Valentine et al, 2004; in adulthood dramatic changes in topographic maps can occur. Relatively short-duration and localized changes in primary auditory cortex can be caused by intracortical microstimulation (Valentine and Eggermont, 2003), but more dramatic ones can follow electrical kindling (Valentine et al, 2004).…”

“…Relatively short-duration and localized changes in primary auditory cortex can be caused by intracortical microstimulation (Valentine and Eggermont, 2003), but more dramatic ones can follow electrical kindling (Valentine et al, 2004). In the latter case large parts of auditory cortex became tuned to a narrow frequency range and the intracortical synchrony increased dramatically.…”

Experience dependent plasticity alters cortical synchronization

“…Selective attention, behavioral training, and electrical kindling can simultaneously increase synchronization and decrease receptive Weld size (Fries et al, 2001;Luck et al, 1997;Gassanov et al, 1985;Steinmetz et al, 2000;Vaadia et al, 1995;Schoenbaum et al, 2000;Sakurai, 1993;Schieber, 2002;Salazar et al, 2004;Valentine et al, 2004). Pairing NB stimulation with noise burst trains causes receptive Welds to increase but decreases the amount of synchrony between A1 recording sites (Bao et al, 2003).…”