Formation of spike response to sound tones in cat auditory cortex neurons: Interaction of excitatory and inhibitory effects

https://doi.org/10.1016/0306-4522(91)90295-YGet rights and content

Abstract

Responses of the auditory cortical neurons to sound tones were studied extra- and intracellularly in anaesthetized cats. The pattern of response to tone stimuli could most differ in neurons tuned to the same sound frequency and forming a vertical cortical column. Phasic reactions were found in 69% of the neurons studied. Such neurons were encountered in all cortical layers but about 50% of them were localized at a depth of 0.4–1.0 mm, which corresponds to layers III and IV of the auditory cortex. Neurons with phasic reactions were able to respond to a relatively narrow frequency band that demonstrates high discriminative ability of these cells to the frequency analysis of sound signals.

Inhibitory processes realized via both forward afferent and recurrent intracortical inhibition mechanisms play particular roles in the formation of phasic reaction of such neurons to different frequency tones. Twenty-six per cent of neurons generated tonic responses to the sound. The majority of such cells (94%) were localized at a depth of 1.0–2.2 mm, which corresponds to cortical layers V and VI. Inhibitory processes exert a much lesser influence on formation of tonic responses in comparison with phasic ones. Neurons of the tonic type, in contrast to phasic neurons, respond to a wider frequency band; their lower ability to discriminate sound frequency is obvious. Parameters of the responses of tonic neurons strictly correlated with the duration and intensity of the acoustic signal. The possibility of some tonic neurons playing an inhibitory rote in auditory cortex is discussed [Volkov I.O. et al. (1989) Neurophysiology, Kiev21, 498–506, 613–620 (in Russian)].

A small portion of the auditory area AI neurons (2%) demonstrated the suppression of background activity during tone stimulation. They were localized mainly in deep cortical layers (V and VI). Intracortical inhibition is supposed to play a dominant role in the formation of this type of response.

About 3% of the studied auditory cortex neurons with background activity generated no response to tonic stimuli. Such cells were usually encountered in the superficial auditory cortex layers (I and II).

References (64)

  • EdelmanG.M. et al.

    The Mindful Brain. Cortical Organization and Group-selective Theory of Higher Brain Function

    (1981)
  • ErulkarS.D. et al.

    Single unit activity in the auditory cortex of the cat

    Bull. Johns Hopkins Hosp.

    (1956)
  • EvansE.F. et al.

    Classification of unit responses in unanaesthetized and unrestrained cat

    J. Physiol.

    (1964)
  • GenisE.D. et al.

    On morphology of the cat auditory cortex

    Neurophysiology, Kiev

    (1973)
  • GershuniG.V.

    Organization of afferent inflow and the process of discrimination of signals of various duration

    Zh. vyssh. nerv. Deyat.

    (1965)
  • GoldsteinM.N. et al.

    Single unit activity in primary auditory cortex of unanaesthetized cats

    J. acoust. Soc. Am.

    (1968)
  • GreenwoodD.D. et al.

    Excitatory and inhibitory response areas of auditory neurons in the cochlear nucleus

    J. Neurophysiol.

    (1965)
  • HartlineH.K. et al.

    Inhibitory interaction of receptor units in the eye of Limulus

    J. gen. Physiol.

    (1957)
  • HellwegF.-C. et al.

    Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation

    J. Neurophysiol.

    (1977)
  • HindJ.E.

    Unit activity in the auditory cortex

  • HubelD.H. et al.

    Functional architecture of macaque monkey cortex

  • JonesE.G.

    Lamination and differential distribution of thalamic afferents within the sensorimotor cortex of the squirrel monkey

    J. comp. Neurol.

    (1975)
  • KatsukiJ. et al.

    Electrical activity of cortex auditory neurons of unanaesthetized and unrestrained cat

  • KatsukiJ. et al.

    Activity of auditory neurons in upper levels of cat brain

    J. Neurophysiol.

    (1959)
  • KiangN.J. et al.

    Stimulus coding in the cochlear nucleus

    Anat. Otol. Rhinol. Laryngol.

    (1965)
  • KiangN.J. et al.

    Stimulus coding in the cat's auditory nerve

    Anat. Otol. Rhinol. Laryngol.

    (1962)
  • KrnjevicˆK. et al.

    Nature of a cortical inhibition process

    J. Physiol.

    (1966)
  • LundJ.S. et al.

    Interlaminar connections and pyramidal neuron organization in the visual cortex area 17 of the macaque monkey

    J. comp. Neurol.

    (1975)
  • McCornickD.A. et al.

    Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex

    J. Neurophysiol.

    (1985)
  • MerzenichM.M. et al.

    Representation of cochlear within primary auditory cortex in the cat

    J. Neurophysiol.

    (1975)
  • MitaniA. et al.

    Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat

    J. comp. Neurol.

    (1985)
  • MountcastleV.B.

    Modality and topographic properties of single neurons of cat's somatic sensory cortex

    J. Neurophysiol.

    (1957)
  • Cited by (0)

    View full text