Elsevier

Neuropharmacology

Volume 37, Issues 4–5, 5 April 1998, Pages 581-592
Neuropharmacology

Long-term potentiation in vivo in layers II/III of rat barrel cortex

https://doi.org/10.1016/S0028-3908(98)00039-2Get rights and content

Abstract

Long-term potentiation was studied in vivo in the rat barrel cortex. It was found that LTP lasting several hours could be induced in layer II/III by tetanic stimuli applied in layer IV. The probability of inducing LTP at a given site was high (86%) provided that the electrodes were not displaced too far horizontally. LTP was not observed if the stimulating electrode was located on the far side of the neighbouring barrel-column from the recording electrode. The strongest LTP was induced by stimulating layer IV septal locations or the edge of the barrel and recording in the near half of the neighbouring barrel. However, examples were found of LTP from layer IV to II/III within the same barrel, within the same septum and from barrel to adjacent septum. The probability of inducing LTP on a particular occasion was greatly increased by iontophoresis of bicuculline at the recording site during the tetanus (from 20 to 55% judged by a change in peak amplitude). The average increase in the peak amplitude was 29±3.2% for protocol 1 (urethane anesthesia, monopolar stimulation) and 23±7% for protocol 2 (barbiturate anesthesia, bipolar stimulation). The probability of inducing LTP was greater if the first tetanus was accompanied by BMI application (67%) than for any subsequent attempts (39%). These results suggest it should be possible to study the effect of LTP on sensory processing in defined positions within the barrel field.

Introduction

The first full reports of long-term potentiation (LTP) in the hippocampus described LTP in vivo (Bliss and Gardner-Medwin, 1973, Bliss and Lomo, 1973). LTP was not studied in the in vitro slice preparation until later (Anderson et al., 1977). In the neocortex, LTP has been studied both in vivo (Sakamoto et al., 1987, Voronin, 1984, Lee and Ebner, 1992, Tamura et al., 1992, Heynen et al., 1996) and in vitro (Artola and Singer, 1987, Komatsu et al., 1988, Perkins and Teyler, 1988). However, there are still comparatively few studies of LTP in vivo in the neocortex, perhaps due to the advantages of the slice preparation and the complexity of the in vivo preparation. One obvious advantage of studying LTP in vivo is the ability to look at the effect of LTP on sensory information processing. However, there are a number of clear difficulties, notably the problem of placing the stimulating and recording electrodes accurately and repeatedly in the optimal position for inducing LTP. In this study, we have attempted to overcome some of these problems by studying LTP in the barrel cortex. The receptive fields of the barrel field neurones and their response latencies to stimulation of the vibrissae can be used to determine approximately where the electrodes are located within the cortex with respect to cortical layer and cortical barrel-column (Armstrong-James and Fox, 1987). Furthermore, the cortical columns corresponding to each vibrissa can be visualized in layer IV post-hoc using simple histochemical methods, allowing the electrode positions to be verified post-mortem. Electrode position is likely to be an important factor in the induction of LTP due to the heterogeneity of cell type in the cortex and the complexity of the cortical structure in general.

Different layers in the cortex show different degrees of plasticity. For example, monocular deprivation experiments and vibrissae deprivation experiments show that layer IV is most plastic early in life and layers II/III later (see Fox, 1996). Similarly, thalamocortical synapses have a very short critical period for LTP in the barrel field (Crair and Malenka, 1995) while LTP can be induced into adulthood in superficial layers of visual (Komatsu et al., 1988) and barrel cortex (Aroniadou-Anderjaska and Keller, 1995). We decided therefore, to study induction of LTP in layers II/III by stimulating layer IV. A number of reports have shown that in the slice preparation LTP can be induced without disinhibition by theta burst stimulation applied to layer IV (Kirkwood and Bear, 1994, Castro-Alamancos et al., 1995). We therefore studied the efficacy of a number of induction protocols, including theta burst stimulation.

This report is a description of the conditions under which LTP was produced and the likelihood of induction from particular sites. In this first study we have concerned ourselves with the questions of whether there are preferential sites for induction of LTP in the cortex, whether disinhibition is required and how long LTP lasts in this structure. We show that LTP can be induced in layers II/III of the barrel cortex, both within barrels and between barrels, although many factors interact to determine whether LTP will take place at a particular site. These studies should facilitate future investigations into the consequences of LTP for sensory information processing.

Section snippets

Subjects

Subjects were male and female Long-Evans rats aged 21–42 days. A group of 43 animals was used.

Anaesthesia and surgery

Anaesthesia was induced with metofane (Mallinckrodt, US) and maintained with i.p. injections of urethane (1.5 g/kg of body weight, Aldrich) or barbiturate (Sagatal, 65 mg/kg of body weight, Rhone Merieux). Depth of anaesthesia was monitored by testing hindlimb reflexes and observing the EEG. Animals were reinjected with 10% of the initial dose of anaesthetic if the hindlimb reflex was brisk and/or if

Results

Two sets of experiments were performed in this study in an attempt to find optimal conditions for LTP. In the first series, we studied LTP induction in urethane anaesthetised animals and used single barrel carbon fibre microelectrodes for monopolar stimulation (protocol 1). In the second series of experiments, we studied LTP in barbiturate anaesthetised animals and used dual carbon fibre microelectrodes for bipolar stimulation (protocol 2). The two data sets are described separately below.

Discussion

The results demonstrate that LTP can be induced in the barrel cortex in vivo. Provided the stimulating electrode was located in layer IV or the bottom of layer III and the recording electrode superficial to it, LTP could be produced in pathways between barrels, between septum and barrel between barrel and septum, and within either the same septal compartment or the same barrel-column.

The average size of potentiation was comparable with reports in the literature for in vivo LTP in the dentate

Acknowledgements

We should like to express thanks to Xinren Li for preparing the histology on the early experiments in this study. This work was supported by NIH grant NS27759 to KF and by grants from the United Kingdom’s MRC to KF and to PC.

References (28)

  • M Armstrong-James et al.

    A method for etching the tips of carbon fibre microelectrodes

    J. Neurosci. Methods

    (1980)
  • T Sakamoto et al.

    Long lasting potentiation of potentials in the motor cortex produced by stimulation of the sensory cortex in the cat

    Brain Res.

    (1987)
  • C.D Aizenman et al.

    A current source density analysis of evoked responses in slices of adult rat visual cortex: Implications for the regulation of long-term potentiation

    Cereb. Cortex

    (1996)
  • P Anderson et al.

    Specific long-lasting potentiation of synaptic transmission in hippocampal slices

    Nature

    (1977)
  • M Armstrong-James et al.

    Spatiotemporal convergence and divergence in the rat S1 ‘barrel’ cortex

    J. Comp. Neurol.

    (1987)
  • V Aroniadou-Anderjaska et al.

    LTP in the barrel cortex of adult rats

    Neuroreport

    (1995)
  • A Artola et al.

    Long-term potentiation and NMDA receptors in rat visual cortex

    Nature

    (1987)
  • D.M Bannerman et al.

    Inhibition of nitric oxide synthase does not prevent the induction of long-term potentiation in vivo

    J. Neurosci.

    (1994)
  • T.V.P Bliss et al.

    Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path

    J. Physiol.

    (1973)
  • T.V.P Bliss et al.

    Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestheized rabbit following stimulation of the perforant path

    J. Physiol.

    (1973)
  • M.A Castro-Alamancos et al.

    Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex

    J. Neurosci.

    (1995)
  • M.C Crair et al.

    A critical period for long-term potentiation at thalamocortical synapses

    Nature

    (1995)
  • N.W Daw et al.

    Critical period for monocular deprivation in the cat visual cortex

    J. Neurophysiol.

    (1992)
  • K Fox

    A critical period for experience-dependent synaptic plasticity in rat barrel cortex

    J. Neurosci.

    (1992)
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