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Lateral Inhibition

Lateral inhibition, is a decrease in response in neurons that occurs when neighboring neurons become activated. For example, in Figure 1(a), a network of 10 excitatory neurons receiving information from visual space (such as neurons in the retina or later levels of the visual system) is intermingled with 9 inhibitory neurons. Activity in any one of the excitatory neurons can inhibit its neighbors indirectly by activating the inhibitory neurons that then inhibit their neighbors. When a stimulus (such as a bar of light or any other stimulus) excites a number of neurons in the network (in this case neurons 4e, 5e, 6e, and 7e), the effect of inhibition is to suppress the neurons just outside the edge of the bar (3e and 8e) because those neurons are inhibited but not excited. Further, because the neurons just inside the edges of the bar (4e and 7e) are excited by light and only inhibited by one neighbor, they are especially active. This leads to perceptual contrast enhancement at borders. Further research showed that lateral inhibition also applied to overlapping stimuli, and that its strength fell off with distance between the interacting stimuli.

Haldan Keffer Hartline won the Nobel Prize in 1967 for discovering lateral inhibition and its neural correlates. The first inhibitory circuit in the nervous system was found in the horseshoe crab (Limulus polyphemus). Here, an activated photo-receptor was inhibited when a laterally adjacent (or nearby) photoreceptor was also activated. Lateral inhibitory circuits are currently known to be ubiquitous to all sensory areas of the brain, and they play an important role in many sensory, cognitive, motor, affective, and limbic processes. The most common mechanism by which neurons suppress their neighbors is through the inhibitory neurotransmitter gamma-aminobutyric acid (GABA).

Hartline and his collaborator, Floyd Ratliff, went on to characterize the three components of a laterally inhibitory circuit: (1) Excitatory input and output—information input arrives at a given sensory area of the brain in the form of excitatory neural responses. Information output is sent to the next area(s) in the hierarchy also in the form of excitatory neural responses; (2) Self-inhibition—neurons that laterally inhibit their neighbors also inhibit themselves; (3) Lateral inhibition occurs as a function of excitatory activation—thus inhibition follows excitation in time.

The Role of Lateral Inhibition through Time

In addition to its effects across space, lateral inhibition also leads to temporal effects over time. Let us now examine two neurons embedded within a lateral inhibitory network as a function of time (Figure 1b): one excitatory neuron (at times 1e through 10e) and its connected inhibitory neuron (at times 1i through 9i). At times 1e, 2e, and 3e (before the stimulus is presented), there is no excitatory input, so the output remains flat. At time 4e (just after the stimulus, such as a bar of light, is presented), the neuron is excited, causing an onset-response. This leads to the activation of the inhibitory neuron at time 4i, after a slight delay. The inhibitory neuron then feeds back on the excitatory neuron and causes its activity to be suppressed at time 5e. This state of excitatory-inhibitory equilibrium is called the sustained period, which continues through time 7e, after which the stimulus is extinguished. Despite the stimulus having been terminated, the neuron at time 7i is nevertheless activated by the excitatory neuron at time 7e because of the delayed effect of inhibition. Thus, the excitatory neuron at time 8e is inhibited while not being excited by visual input, and so is in a state of deep suppression called the time-out period, which in turn causes the inhibitory neuron at time 8i to be deeply suppressed because of lack of input. The excitatory neuron at time 9e then exhibits a disinhibitory rebound called the after-discharge because of the lack of baseline inhibition (even though there is no excitatory input).

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