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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

Non-specific tic-related neuronal activity. Schematic illustration depicting the relative frequency and spatial distribution of neuronal activity patterns in the cortico-basal ganglia system related to motor tics confined to a single muscle group (Bronfeld et al., 2011). In the striatum, tic-related activity was confined to the somatotopical territory of the tic location, but almost all projection neurons recorded from that territory displayed non-specific tic-related bursts of activity. In the pallidum, tic-related activity was detected in a very large and spatially diffuse subpopulation of neurons. Tic-related excitations and inhibitions were the predominant responses in GPe and GPi neurons, respectively.
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Figure 2: Non-specific tic-related neuronal activity. Schematic illustration depicting the relative frequency and spatial distribution of neuronal activity patterns in the cortico-basal ganglia system related to motor tics confined to a single muscle group (Bronfeld et al., 2011). In the striatum, tic-related activity was confined to the somatotopical territory of the tic location, but almost all projection neurons recorded from that territory displayed non-specific tic-related bursts of activity. In the pallidum, tic-related activity was detected in a very large and spatially diffuse subpopulation of neurons. Tic-related excitations and inhibitions were the predominant responses in GPe and GPi neurons, respectively.

Mentions: Motor tics are repetitive involuntary brief muscle contractions that can appear either as the primary or a secondary symptom in several human movement disorders, most notably Tourette syndrome (TS; Kurlan, 2004). Tics are primarily associated with dysfunction of the BG input structure – the striatum (Singer and Minzer, 2003). Our studies (McCairn et al., 2009; Bronfeld et al., 2011) of BG neuronal activity in a non-human primate model of motor tics suggested that tics were also associated with BG LOS (Figure 2). In the striatum, tic-related activity was somatotopically organized, but almost all neurons recorded from the tic-related somatotopical territory displayed non-specific tic-related activity (Bronfeld et al., 2011). In the GPe and GPi, a larger than normal fraction of recorded neurons (over 70%) demonstrated strong activity modulations related to tic-movements, even though tics were confined to one or a few muscles (McCairn et al., 2009). Similar findings were observed in the GPi of TS patients undergoing neurosurgery (Zhuang et al., 2009). Tic-related neurons were diffusely distributed within GPe and GPi, with no spatial organization of neurons expressing similar types of tic-related activity (Figure 2), suggesting a loss of the somatotopic organization in these structures (McCairn et al., 2009; Zhuang et al., 2009).


Loss of specificity in Basal Ganglia related movement disorders.

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

Non-specific tic-related neuronal activity. Schematic illustration depicting the relative frequency and spatial distribution of neuronal activity patterns in the cortico-basal ganglia system related to motor tics confined to a single muscle group (Bronfeld et al., 2011). In the striatum, tic-related activity was confined to the somatotopical territory of the tic location, but almost all projection neurons recorded from that territory displayed non-specific tic-related bursts of activity. In the pallidum, tic-related activity was detected in a very large and spatially diffuse subpopulation of neurons. Tic-related excitations and inhibitions were the predominant responses in GPe and GPi neurons, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Non-specific tic-related neuronal activity. Schematic illustration depicting the relative frequency and spatial distribution of neuronal activity patterns in the cortico-basal ganglia system related to motor tics confined to a single muscle group (Bronfeld et al., 2011). In the striatum, tic-related activity was confined to the somatotopical territory of the tic location, but almost all projection neurons recorded from that territory displayed non-specific tic-related bursts of activity. In the pallidum, tic-related activity was detected in a very large and spatially diffuse subpopulation of neurons. Tic-related excitations and inhibitions were the predominant responses in GPe and GPi neurons, respectively.
Mentions: Motor tics are repetitive involuntary brief muscle contractions that can appear either as the primary or a secondary symptom in several human movement disorders, most notably Tourette syndrome (TS; Kurlan, 2004). Tics are primarily associated with dysfunction of the BG input structure – the striatum (Singer and Minzer, 2003). Our studies (McCairn et al., 2009; Bronfeld et al., 2011) of BG neuronal activity in a non-human primate model of motor tics suggested that tics were also associated with BG LOS (Figure 2). In the striatum, tic-related activity was somatotopically organized, but almost all neurons recorded from the tic-related somatotopical territory displayed non-specific tic-related activity (Bronfeld et al., 2011). In the GPe and GPi, a larger than normal fraction of recorded neurons (over 70%) demonstrated strong activity modulations related to tic-movements, even though tics were confined to one or a few muscles (McCairn et al., 2009). Similar findings were observed in the GPi of TS patients undergoing neurosurgery (Zhuang et al., 2009). Tic-related neurons were diffusely distributed within GPe and GPi, with no spatial organization of neurons expressing similar types of tic-related activity (Figure 2), suggesting a loss of the somatotopic organization in these structures (McCairn et al., 2009; Zhuang et al., 2009).

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