Effects of ketamine on synaptic transmission and long-term potentiation in layer II/III of rat visual cortex in vitro
Introduction
It has long been assumed that lasting modifications of synaptic transmission form a basis for information storage in the nervous system, and that modifications subserving certain forms of learning and memory are likely to reside in the cerebral neocortex (Hebb, 1949). Since the initial discovery of long-term potentiation by Bliss and Lømo (1973), the process has been studied intensively in the hippocampus (Bliss and Collingridge, 1993). Long-term potentiation has also been investigated, although less intensively, in the neocortex particularly in the visual cortex.
According to present evidence, very similar mechanisms mediate synaptic plasticity in the hippocampal CA1 area and the visual cortex. The visual cortex offers an important, perhaps unique, advantage over the CA1 for the eventual understanding of how long-term potentiation and long-term depression contribute to the functioning of the brain. This advantage is that the visual cortex lies much closer to the interface between electrophysiology and behavior than does the hippocampus (Kirkwood and Bear, 1995).
Electrical stimulation of white matter, intracellular recordings (Sutor and Hablitz, 1989), and field potential recordings (Aroniadou and Teyler, 1991) have shown that there are two types of excitatory postsynaptic potentials (EPSPs) in layer II/III of the visual cortex: a low-threshold and short latency EPSP and a high-threshold and long latency EPSP, which are called excitatory postsynaptic potential1 (EPSP1) and excitatory postsynaptic potential2 (EPSP2), respectively. The EPSP1 is a monosynaptic response and, in turn, it includes EPSP1a and EPSP1b, which are mediated by non-NMDA and NMDA receptors, respectively. The EPSP2 is probably a polysynaptic response and present evidence indicates that NMDA receptor-dependent and -independent EPSP2 can exist (Aroniadou and Teyler, 1991). In addition, inhibitory postsynaptic potentials (IPSP) have been demonstrated in layer II/III of the visual cortex including a fast IPSP and a slow IPSP that are mediated by GABAA and GABAB receptors, respectively (Connors et al., 1988).
Previous studies have generally emphasized that long-term potentiation cannot readily be elicited in the visual cortex from adult rats, especially in the absence of a GABA blocker Artola and Singer, 1987, Kimura et al., 1989, Kato et al., 1991. Application of high-frequency electrical stimulation to the pathway of interest can induce long-term potentiation. Among the different patterns of tetanic stimulation, theta-burst stimulation and primed-burst stimulation may particularly be important. These protocols mimic the synchronized firing patterns at frequencies that occur in the hippocampus of rats during learning (Bliss and Collingridge, 1993), but it is not clear whether this is also true for the visual cortex. However, experimental data indicate that theta-burst stimulation is an effective stimulation protocol for neocortical potentiation Kirkwood and Bear, 1994, Castro-Alamancos and Connors, 1996.
It has been shown that NMDA receptors are involved in neocortical long-term potentiation. Artola and Singer (1990) found that NMDA receptor-specific antagonists are able to block long-term potentiation of the EPSP. Findings of different laboratories show that dl-2-amino-5-phosphono-valeric acid (AP5), an NMDA receptor antagonist, inhibits NMDA receptor-mediated long-term potentiation Kimura et al., 1989, Artola and Singer, 1990, Lee et al., 1991, Bear et al., 1992. However, Komatsu et al. (1991) reported that tetanic stimulation in the presence of AP5, in some cases, led to long-term potentiation; 6,7-dinitroquinoxaline-2,3(1H,4H)-dione (DNQX), a non-NMDA receptor antagonist, eliminated this potentiation. This type of potentiatoin has also been reported by Aroniadou and Teyler (1991).
Ketamine (2-O-chlorophenyl-2-methylaminocyclohexanone), which is pharmacologically similar to MK-801, blocks NMDA receptors in a use-dependent mode and the blockade is enhanced by the presence of agonist (Gonzales et al., 1995). It blocks NMDA receptors in closed and open states (Orser and Freeman, 1997). This action is thought to contribute to potent anesthetic and analgesic properties of ketamine (Irifune et al., 1992). Ketamine can also interfere with synaptic consolidation in the visual cortex (Rauschecker et al., 1990) and inhibits NMDA receptor-dependent EPSP in the cerebral cortex (Thomson et al., 1985). It also blocks glutamate receptors that are activated by quisqualate (Gonzales et al., 1995). But AP5 is a competitive NMDA receptor antagonist that acts on the transmitter recognition site of the receptor and prevents receptor activation by competing with the agonist for the transmitter-binding site (MacDonald and Nowak, 1990).
Until now, the effects of ketamine on long-term potentiation in the visual cortex have not been established. Therefore, the effects of ketamine on the induction and maintenance of long-term potentiation induced by primed-burst stimulation in the visual cortex were investigated in vitro.
Section snippets
Animals
Visual cortex slices were prepared from male and female NMRI rats ranging from 4–6 weeks of age. As long-term potentiation was found to be unrelated to the sex of the animal (Berry et al., 1989), data from the two sexes were pooled. Fifteen slices from 12 rats and 14 slices from 10 rats were used in control and ketamine experiments, respectively. Animals were housed in a standard environment on a 12:12 h light/dark cycle at 22±2°C. Animals were allowed access to water and food ad libitum.
Slice preparation
Slices
Baseline recording in layer II/III of visual cortex
Stimulation of layer IV resulted in a two-component response in layer II/III at 25 μA stimulus intensity. Both components were eliminated in Ca2+-free medium (Fig. 1). The first component had a short latency (1.25±0.11 ms) and high amplitude (2±0.3 mV) and the second component had a long latency (3.94±0.23 ms) and low amplitude (0.9±0.2 mV). A high stimulus intensity (200 μA) differently influenced the baseline response. Whereas the amplitude of the first component increased without exception,
Baseline recordings
The analysis of field potential data has been rigorously discussed in the literature Berry et al., 1989, Aroniadou and Teyler, 1991, Aizenman et al., 1996, Castro-Alamancos and Connors, 1996. We used field potentials to assess the effect of ketamine on the plasticity of synaptic connections in layer II/III of rat visual cortex in vitro, in response to primed-burst stimulation, as a type of activity pattern, that is extensively used to study the plasticity of synaptic connections in the
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