Orienting Response Research Paper

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1. The Concept Of Orienting Response

The orienting response (OR), discovered by Pavlov (1927), is a set of reactions evoked in humans and animals by a novel stimulus. The OR is manifested in an interruption of an ongoing activity (an external inhibition) that parallels turning of eyes, head, and body movements toward a novel stimulus (the targeting response) (Konorski 1967). Subjectively, the OR is experienced as an involuntary switching of attention emphasizing a novel stimulus.

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2. Components Of OR

The behavioral manifestations of OR represent only the tip of an iceberg of reactions hidden from direct observation but revealed by instrumental research. OR is characterized by a constriction of peripherical vessels and dilation of brain vessels. The regional cerebral blood flow (rCBF) is of particular interest, being related to a local activation of neurons expressed in the generation of action potentials (APs). APs are linked with passive inflow of sodium and outflow of potassium ions from nervous cells. To keep a balance of ionic content in neurons an active sodium-potassium pump is operating. It requires additional energy supplied by oxygen and glucose during the intensification of rCBF. The increase of rCBF as an index of OR-related neuronal activation is used in positron emission tomography (PET) and functional magnetic resonance imaging (f MRI).

Neuronal networks involved in OR evocation are identified also by electroencephalography (EEG) and magneto encephalography (MEG) (Posner and Raichle 1994). Multichannel EEG and MEG recordings are used to calculate equivalent dipoles localization representing loci of neuronal activation. OR is evident as event-related desynchronization (ERD) of background brain waves in the range of 8 to 12 Hz (alpha waves) that parallels an increase of beta (12 to 25 Hz) and gamma (25 to 200 Hz) oscillations (Naatanen 1992). The ERD is accompanied by a negative shift of the cortical steady potential that is related to an increase in neuronal excitability (Caspers 1963). The other OR index is nonspecific event-related potentials (ERPs) evoked by novel stimuli (Brunia 1997).

Direct observation of OR-related neurons is done by single unit microelectrode recording. The OR is also expressed in autonomic indicators: deceleration of heart rate and an increase of skin conductance (Graham 1979). Sensory OR components refer to an elevation of sensitivity (lowering of thresholds) and to an increase of fusion frequency (rate of discrete stimuli building up a continuous percept) (Lindsley 1961).

3. Selective Habituation Of OR

Repeated presentation of a nonsignal standard stimulus results in a gradual reduction of OR components (OR habituation). The OR habituation represents a form of negative learning. A change of the presented stimulus produces OR, again demonstrating the contribution of novelty. A standard stimulus following a novel one results in OR recovery called dishabituation (Groves and Thompson 1970). The standard stimulus characterized by a particular intensity, shape, color, duration, and interstimulus intervals builds up in neuronal networks an internal representation of all these parameters—a stimulus neuronal model. Any deviation of a stimulus from the created neuronal model produces a mismatch signal that determines OR generation. The stimulus neuronal model preserves not only simple features, but also their combinations. Thus, after habituation of OR to a complex consisting of light and sound components, elimination of either light or sound evokes OR.

The stimulus neuronal model can be characterized as a multidimensional self-adjustable reject filter. A selective tuning of the filter can be revealed by repeated presentation of the standard stimulus and intermittent stimuli deviating with respect to a particular parameter from the standard one.

The procedure applied to different stimulus parameters enables the construction of a multidimensional filter with a selective characteristic that underlies stimulus selective OR habituation. Repeated presentation of a standard stimulus reveals generalized and localized ORs. Generalized OR is evident by the involvement of a wide variety of components that rapidly habituate. Localized OR is specifically related to the applied stimulus modality. Generalized and localized ORs can be demonstrated by event-related desynchronization (ERD) of brain waves. Different brain areas are represented by specific alpha, mu, sigma, and tau generators of 8 to 12 Hz oscillations. The visual area is represented by alpha rhythm, the motor area by mu rhythm, the somatosensory area by sigma rhythm, and the auditory area by tau rhythm. A novel visual stimulus evokes a generalized OR composed of generalized ERD, skin galvanic response (SGR), and heart rate deceleration. After 15 to 20 presentations of the visual stimulus only occipital alpha-desynchronization is seen being habituated in subsequent trials. Passive hand movement produces initially a generalized ERD that under repetitions is transformed into a local mu rhythm desynchronization representing a localized OR (Sokolov 1963).

4. OR And Conditioned Reflex

A combination of neuronal (nonsignal) stimulus with an unconditional stimulus (US) results in an intensification of OR. The stimulus signaling a US becomes significant and produces more stable OR. In the process of stabilization of the conditional reflex (CR) the OR gradually habituates. An additional stumble, that has to be differentiated from the initial CS, results in a recovery of OR. The more difficult the differentiation task, the greater is the OR. If CSs are presented at regular intervals, a time-selective CR is elaborated that precedes actual presentation of the CS. It parallels an anticipatory OR expressed in saccadic eye movements, ERD and gradual negative shift of study potential (expectancy wave). Thus nonsignal (insignificant) stimuli produce rapidly habituatable OR, while signal (significant) stimuli triggers produce more persistent OR.

5. OR And Vector Encoding

A stimulus acting on an ensemble of receptors generates a combination of their excitations—a receptor excitation vector. The receptors’ overlapping characteristics constitute a nonorthogonal basis. At the next stage of information processing the neuronal ensemble performs orthogonalization and normalization so that input stimuli are represented in Euclidean space by excitation vectors of a constant length.

An excitation vector evoked by an input stimulus is acting in parallel on a set of feature detectors. Each feature detector is selectively tuned to a particular excitation vector and in this way maximally excited by a respective input stimulus. Thus input stimuli encoded by excitation vectors are topically represented on a detector map. The detector map is a hypersphere in a multidimensional space. The output responses are also encoded by means of excitation vectors. A variety of specific responses can be generated by a limited number of channels constituting components of an output excitation vector (Bizzi and Mussa-Ivaldi 1998). A link between input and output excitation vectors having a set of plastic synapses modified in the process of learning so that command neuron become selectively tuned to a CS (Fomin et al. 1979).

The OR habituation as a negative learning is also due to the synaptic plasticity of specific novelty-related command neurons. The process of OR selective habituation can be explained by the formation of a Hebbian link vector opposing an excitation vector of a standard stimulus (Hebb 1949).

The model of OR information processing presented above can be illustrated by color vision. Three types of cones constitute a nonorthogonal basis for receptor excitation vectors. Three types of photopic horizontal cells, red-green, blue-yellow, and luminance, are relevant for the orthogonal basis, where intensity is given by the vector length. At the level of bipolar cells the length of excitation vectors becomes constant. This is achieved by a transition from a three to a fourdimensional space with the addition of a neuron active under darkness. At color specific visual area (V4) different colors are specified by color-selective detectors (Bartles and Zeki 1998). The color detector map is a hypersphere in the four-dimensional space (Izmailov and Sokolov 1991). The spherical surface representing colors suggests that different colors be topically separated, constituting a colortopic cortical map similar to retinatopic, tonotopic, and somatotopic projections. An f MRI used to localize color representations reveals color-selective areas in the human occipitotemporal cortex.

Output vector code is evident in different ballistic movements (Bizzi and Mussa-Ivaldi 1998). OR vector code is expressed in saccadic eye movements, which are selectively triggered by particular combinations of horizontal, vertical, and torsion premotor neurons. Vector code refers to autonomic OR response (Sokolov and Cacioppo 1997).

6. Neuronal Basis Of OR

PET and f MRI in combination with EEG and MEG studies in humans have shown that OR circuits differ in passive (involuntary) and active (voluntary) OR. Passive OR is addressed to the hippocampus (Tulving et al. 1994) while active OR involves the prefrontal and parietal lobes. Single unit recording in the hippocampus of a rabbit has demonstrated that neurons under passive OR are separated into two groups. Novelty-sensitive neurons are excited by a novel stimulus. Familiarity-sensitive neurons are inhibited by a novel stimulus. By repeated presentation of a novel stimulus responses of excitatory and inhibitory cells are habituated.

Selective habituation with respect to a standard stimulus is due to a selective decrease of synaptic weights connecting activated feature detectors with novelty-related neurons (Vinogradova 1987). The mismatch signal evoked by the noncoincidence of a stimulus deviating from the standard one parallels a difference of their excitation vectors. The mismatch signal is addressed to the mesencephalic reticular formation and thalamic reticular nuclei evoking a frequency shift of their pacemaker cells from alpha waves (Moruzzi and Magoun 1949) toward gamma oscillations. Single unit recording from the reticular thalamic nucleus in rabbits demonstrates randomization response—a transition from bursting spike activity to a random spiking that parallels ERD of cortical alpha-like oscillations. By repeated presentation of a novel stimulus, neuron spiking thalamic randomization response and ERD selectively habituate in accordance with the stimulus selective habituation of other OR components (Sokolov 1975).

The hippocampus plays a distinct role in the orienting reflex and exploratory behavior. The hippocampus is characterized by (a) long-term potentiation of synaptic contacts; (b) hippocampal theta waves (4 to 7 Hz) during arousal and orienting reaction; (c) novelty and familiarity neurons.

Cortical future detectors reach the hippocampus via the perforant path contacting apical dendrites of pyramidal cells. In passing, individual fibers make numerous contacts with many pyramidal cells so that excitation is spread over a wide area of the hippocampus. A parallel branch of the perforant path contacts granule cells of the dentate fascia, which sends its mossy fibers to basal dendrites of the pyramidal cells. The potentiation of the mossy fibers’ synapses gradually blocks direct synaptic contacts so that the input signal on the pyramidal neurons is selectively diminished. A new stimulus acting via synapses not blocked by the mossy fibers evokes novelty responses in the pyramidal cells that trigger OR.

A critical role of the dentate fascia in the process of habituation was shown using antibodies against neurons of the dentate fascia. This procedure results in an elimination of novelty responses. The novelty neurons become continually responsive under repeated stimulus presentation (Vinogradova 1987).

To summarize: OR is a neuronal mechanism emphasizing novel and significant stimuli against familiar and insignificant ones. One might say that OR is a high order contrasting mechanism contributing to long-term memory formation.

7. Conclusion

Neurons demonstrate basic characteristics of OR. They selectively habituate to different Single unit recording in animals demonstrated that hippocampal novelty-sensitive parameters of the standard stimulus respond to any change of stimulation and show dishabituation. In the hippocampus, familiarity-sensitive neurons are operating in parallel with the novelty-sensitive neurons.

Recent f MRI data show that the human hippocampus is also processing both novelty and familiarity. The left anterior hippocampus responds to perceptual and semantic novelty. By contrast, the bilateral posterior hippocampus is activated by increasing semantic familiarity. Repeated presentation of semantic stimuli results in the topographical spread of hippocampal activity in an anterior–posterior direction. The specific novelty-encoding path plays a crucial role in formation of long-term memory within the posterior medialtemporal lobe (Strange et al. 1999). PET, f MRI, and ERPs show that under active attention task additionally frontal and parietal areas, the anterior cingulate gyrus on the frontal midline are activated, demonstrating that active OR to signal stimuli has a specific circuitry differing from passive OR (Mountcastle 1979).

A novelty signal is widely distributed among different brain structures including the activating reticular formation, autonomic centers, and superior colliculus, facilitating eye and body movements as OR components. At the same time, the novelty signal acts as a distracter of ongoing behavior.


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