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Loss of specificity in Basal Ganglia related movement disorders.

Bronfeld M, Bar-Gad I - Front Syst Neurosci (2011)

Bottom Line: Studies of normal behavior have found that BG neurons tend to phasically modulate their activity in relation to different behavioral events.We review the existing evidence for LOS in BG-related movement disorders, the possible neural mechanisms underlying LOS, its effects on frequently used measures of neuronal activity and its relation to theoretical models of the BG.Thus, the concept of neuronal specificity may underlie a unifying conceptual framework for the BG role in normal and abnormal motor control.

View Article: PubMed Central - PubMed

Affiliation: The Leslie and Susan Gonda (Goldschmied) Multidisciplinary Brain Research Center, Bar-Ilan University Ramat-Gan, Israel.

ABSTRACT
The basal ganglia (BG) are a group of interconnected nuclei which play a pivotal part in limbic, associative, and motor functions. This role is mirrored by the wide range of motor and behavioral abnormalities directly resulting from dysfunction of the BG. Studies of normal behavior have found that BG neurons tend to phasically modulate their activity in relation to different behavioral events. In the normal BG, this modulation is highly specific, with each neuron related only to a small subset of behavioral events depending on specific combinations of movement parameters and context. In many pathological conditions involving BG dysfunction and motor abnormalities, this neuronal specificity is lost. Loss of specificity (LOS) manifests in neuronal activity related to a larger spectrum of events and consequently a large overlap of movement-related activation patterns between different neurons. We review the existing evidence for LOS in BG-related movement disorders, the possible neural mechanisms underlying LOS, its effects on frequently used measures of neuronal activity and its relation to theoretical models of the BG. The prevalence of LOS in a many BG-related disorders suggests that neuronal specificity may represent a key feature of normal information processing in the BG system. Thus, the concept of neuronal specificity may underlie a unifying conceptual framework for the BG role in normal and abnormal motor control.

No MeSH data available.


Related in: MedlinePlus

Effect of loss of specificity on properties of neuronal activity. (A) Illustration of firing rate fluctuations of multiple neurons, depicting rate modulations related to different movements, in a neuronal population for which rate increases are the predominant pattern of movement-related activity. Left: Specific encoding, each neuron modulates its firing rate in response to a single type of movement. Right: Loss of specificity (LOS); each neuron displays similar movement-related rate modulations in response to a larger range of movements. (B) Following LOS, the fraction of movement-related neurons is increased. (C) The number of movements eliciting rate modulations in each neuron increases, resulting in an increased effect of movements on the overall average firing rate of each neuron (i). For a population in which most neurons have a dominant non-specific response pattern (such as firing rate increase), LOS has an effect on the overall average firing rate of the population (ii). (D) Non-specific encoding of movements generates correlations between pairs of neurons (top panel). These correlations represent only the common rate modulations attributed to the commonly encoded movements, and following subtraction of these effects (middle panel, the shift predictor), the normalized correlation function shows no correlation between the neurons (bottom panel).
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Figure 4: Effect of loss of specificity on properties of neuronal activity. (A) Illustration of firing rate fluctuations of multiple neurons, depicting rate modulations related to different movements, in a neuronal population for which rate increases are the predominant pattern of movement-related activity. Left: Specific encoding, each neuron modulates its firing rate in response to a single type of movement. Right: Loss of specificity (LOS); each neuron displays similar movement-related rate modulations in response to a larger range of movements. (B) Following LOS, the fraction of movement-related neurons is increased. (C) The number of movements eliciting rate modulations in each neuron increases, resulting in an increased effect of movements on the overall average firing rate of each neuron (i). For a population in which most neurons have a dominant non-specific response pattern (such as firing rate increase), LOS has an effect on the overall average firing rate of the population (ii). (D) Non-specific encoding of movements generates correlations between pairs of neurons (top panel). These correlations represent only the common rate modulations attributed to the commonly encoded movements, and following subtraction of these effects (middle panel, the shift predictor), the normalized correlation function shows no correlation between the neurons (bottom panel).

Mentions: A widely accepted indicator of LOS is an increase in the fraction of movement-related neurons out of the whole neuronal population. This is based on the premise that in the normal state many neurons which appear to be unrelated to behavior are in fact movement-related, but have a highly selective activity profile, and are therefore unrelated to the specific combination of kinematic and contextual properties of the applied behavioral paradigm (Figure 4A, left). LOS will increase the number of events that each neuron encodes (Figure 4A, right), encompassing a wider range of motor parameters and behavioral paradigms. Under these circumstances neurons that were previously deemed “unrelated” might now demonstrate movement-related activity. This inevitably leads to an increase in the overall number of neurons whose activity is related to any behavioral task (Figure 4B). This measure of LOS has been widely reported in studies of BG-related disorders (see “Neuronal Loss of Specificity” section and Filion et al., 1988; Lenz et al., 1998; Williams et al., 2005; Baker et al., 2010; Erez et al., 2011), but several confounding factors must be taken into account when evaluating its reliability as an indicator of neuronal LOS.


Loss of specificity in Basal Ganglia related movement disorders.

Bronfeld M, Bar-Gad I - Front Syst Neurosci (2011)

Effect of loss of specificity on properties of neuronal activity. (A) Illustration of firing rate fluctuations of multiple neurons, depicting rate modulations related to different movements, in a neuronal population for which rate increases are the predominant pattern of movement-related activity. Left: Specific encoding, each neuron modulates its firing rate in response to a single type of movement. Right: Loss of specificity (LOS); each neuron displays similar movement-related rate modulations in response to a larger range of movements. (B) Following LOS, the fraction of movement-related neurons is increased. (C) The number of movements eliciting rate modulations in each neuron increases, resulting in an increased effect of movements on the overall average firing rate of each neuron (i). For a population in which most neurons have a dominant non-specific response pattern (such as firing rate increase), LOS has an effect on the overall average firing rate of the population (ii). (D) Non-specific encoding of movements generates correlations between pairs of neurons (top panel). These correlations represent only the common rate modulations attributed to the commonly encoded movements, and following subtraction of these effects (middle panel, the shift predictor), the normalized correlation function shows no correlation between the neurons (bottom panel).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3108383&req=5

Figure 4: Effect of loss of specificity on properties of neuronal activity. (A) Illustration of firing rate fluctuations of multiple neurons, depicting rate modulations related to different movements, in a neuronal population for which rate increases are the predominant pattern of movement-related activity. Left: Specific encoding, each neuron modulates its firing rate in response to a single type of movement. Right: Loss of specificity (LOS); each neuron displays similar movement-related rate modulations in response to a larger range of movements. (B) Following LOS, the fraction of movement-related neurons is increased. (C) The number of movements eliciting rate modulations in each neuron increases, resulting in an increased effect of movements on the overall average firing rate of each neuron (i). For a population in which most neurons have a dominant non-specific response pattern (such as firing rate increase), LOS has an effect on the overall average firing rate of the population (ii). (D) Non-specific encoding of movements generates correlations between pairs of neurons (top panel). These correlations represent only the common rate modulations attributed to the commonly encoded movements, and following subtraction of these effects (middle panel, the shift predictor), the normalized correlation function shows no correlation between the neurons (bottom panel).
Mentions: A widely accepted indicator of LOS is an increase in the fraction of movement-related neurons out of the whole neuronal population. This is based on the premise that in the normal state many neurons which appear to be unrelated to behavior are in fact movement-related, but have a highly selective activity profile, and are therefore unrelated to the specific combination of kinematic and contextual properties of the applied behavioral paradigm (Figure 4A, left). LOS will increase the number of events that each neuron encodes (Figure 4A, right), encompassing a wider range of motor parameters and behavioral paradigms. Under these circumstances neurons that were previously deemed “unrelated” might now demonstrate movement-related activity. This inevitably leads to an increase in the overall number of neurons whose activity is related to any behavioral task (Figure 4B). This measure of LOS has been widely reported in studies of BG-related disorders (see “Neuronal Loss of Specificity” section and Filion et al., 1988; Lenz et al., 1998; Williams et al., 2005; Baker et al., 2010; Erez et al., 2011), but several confounding factors must be taken into account when evaluating its reliability as an indicator of neuronal LOS.

Bottom Line: Studies of normal behavior have found that BG neurons tend to phasically modulate their activity in relation to different behavioral events.We review the existing evidence for LOS in BG-related movement disorders, the possible neural mechanisms underlying LOS, its effects on frequently used measures of neuronal activity and its relation to theoretical models of the BG.Thus, the concept of neuronal specificity may underlie a unifying conceptual framework for the BG role in normal and abnormal motor control.

View Article: PubMed Central - PubMed

Affiliation: The Leslie and Susan Gonda (Goldschmied) Multidisciplinary Brain Research Center, Bar-Ilan University Ramat-Gan, Israel.

ABSTRACT
The basal ganglia (BG) are a group of interconnected nuclei which play a pivotal part in limbic, associative, and motor functions. This role is mirrored by the wide range of motor and behavioral abnormalities directly resulting from dysfunction of the BG. Studies of normal behavior have found that BG neurons tend to phasically modulate their activity in relation to different behavioral events. In the normal BG, this modulation is highly specific, with each neuron related only to a small subset of behavioral events depending on specific combinations of movement parameters and context. In many pathological conditions involving BG dysfunction and motor abnormalities, this neuronal specificity is lost. Loss of specificity (LOS) manifests in neuronal activity related to a larger spectrum of events and consequently a large overlap of movement-related activation patterns between different neurons. We review the existing evidence for LOS in BG-related movement disorders, the possible neural mechanisms underlying LOS, its effects on frequently used measures of neuronal activity and its relation to theoretical models of the BG. The prevalence of LOS in a many BG-related disorders suggests that neuronal specificity may represent a key feature of normal information processing in the BG system. Thus, the concept of neuronal specificity may underlie a unifying conceptual framework for the BG role in normal and abnormal motor control.

No MeSH data available.


Related in: MedlinePlus