Imaging Spatiotemporal Dynamics of Surround Inhibition in the Barrels Somatosensory Cortex

Derdikman, Dori; Hildesheim, Rina; Ahissar, Ehud; Arieli, Amos; Grinvald, Amiram

doi:10.1523/jneurosci.23-08-03100.2003

Cited by 162 publications

(142 citation statements)

References 30 publications

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“…The area of cortex activated by a punctate stimulus depends on the sensory modality and the state of the animal; for somatotopic cortex in rat, an ∼3 mm 2 area is found from measurements of net depolarization of cortex stained with a voltage sensitive dye (27). This value coincides with the area of net vasodilation of surface vessels (28), as well as the area of a net oxygenated hemodynamic signal observed by intrinsic optical imaging (39) (Fig.…”

Section: Discussionmentioning

confidence: 59%

“…Lastly, the extent of cortical damage after a permanent block of the MCA is reduced in genetically altered animals with augmented anastomoses in their surface vasculature (19). From the perspective of dynamic resource management, focal somatosensory stimulation, either to a single vibrissa (26,27) or to the forepaw (28), leads to an increase in perfusion at the epicenter of electrical activity in cortex but decreased perfusion in surrounding regions.…”

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confidence: 99%

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Topological basis for the robust distribution of blood to rodent neocortex

Blinder¹,

Shih²,

Rafie³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

165

237

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The maintenance of robust blood flow to the brain is crucial to the health of brain tissue. We examined the pial network of the middle cerebral artery, which distributes blood from the cerebral arteries to the penetrating arterioles that source neocortical microvasculature, to characterize how vascular topology may support such robustness. For both mice and rats, two features dominate the topology. First, interconnected loops span the entire territory sourced by the middle cerebral artery. Although the loops comprise <10% of all branches, they maintain the overall connectivity of the network after multiple breaks. Second, >80% of offshoots from the loops are stubs that end in a single penetrating arteriole, as opposed to trees with multiple penetrating arterioles. We hypothesize that the loops and stubs protect blood flow to the parenchyma from an occlusion in a surface vessel. To test this, we assayed the viability of tissue that was sourced by an individual penetrating arteriole following occlusion of a proximal branch in the surface loop. We observed that neurons remained healthy, even when occlusion led to a reduction in the local blood flow. In contrast, direct blockage of a single penetrating arteriole invariably led to neuronal death and formation of a cyst. Our results show that the surface vasculature functions as a grid for the robust allocation of blood in the event of vascular dysfunction. The combined results of the present and prior studies imply that the pial network reallocates blood in response to changing metabolic needs.anastomoses | imaging | networks | stroke | vasculature

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Section: Discussionmentioning

confidence: 59%

mentioning

confidence: 99%

Topological basis for the robust distribution of blood to rodent neocortex

Blinder¹,

Shih²,

Rafie³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

165

237

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“…4). The earliest response in layer 2͞3 to a single whisker stimulus evokes a region of excitation limited to a single barrel column, which over the subsequent milliseconds can spread to excite the entire barrel cortex (10,14). Based on the membrane potential of the WC recording immediately before the stimulus, sweeps were separated into responses evoked from DOWN states or UP states.…”

Section: Local Glutamatergic Excitation Drives the Up State Which Ismentioning

confidence: 99%

Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex

Petersen

Hahn

Mehta

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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The rodent primary somatosensory cortex is spontaneously active in the form of locally synchronous membrane depolarizations (UP states) separated by quiescent hyperpolarized periods (DOWN states) both under anesthesia and during quiet wakefulness. In vivo whole-cell recordings and tetrode unit recordings were combined with voltage-sensitive dye imaging to analyze the relationship of the activity of individual pyramidal neurons in layer 2͞3 to the ensemble spatiotemporal dynamics of the spontaneous depolarizations. These were either brief and localized to an area of a barrel column or occurred as propagating waves dependent on local glutamatergic synaptic transmission in layer 2͞3. Spontaneous activity inhibited the sensory responses evoked by whisker deflection, accounting almost entirely for the large trial-to-trial variability of sensory-evoked postsynaptic potentials and action potentials. Subthreshold sensory synaptic responses evoked while a cortical area was spontaneously depolarized were smaller, briefer and spatially more confined. Surprisingly, whisker deflections evoked fewer action potentials during the spontaneous depolarizations despite neurons being closer to threshold. The ongoing spontaneous activity thus regulates the amplitude and the time-dependent spread of the sensory response in layer 2͞3 barrel cortex.T he neocortex is spontaneously active. Neocortical neurons in vivo exhibit spontaneous subthreshold membrane potential changes, which can evoke spontaneous action potentials (APs). Such spontaneous activity is not only found in association cortex but is also evident in primary sensory areas. Previous studies have shown that both during slow wave sleep and during anesthesia, the brain state is characterized by low frequency, large amplitude spontaneous membrane potential changes (1-3). Dual intracellular recordings have demonstrated that such spontaneous activity can occur synchronously in nearby neurons (4). Voltage-sensitive dye (VSD) imaging has shown complex patterns of spatiotemporal dynamics of the ensemble spontaneous activity (5-7). The nature of this spontaneous activity and how it interacts with sensory responses is poorly understood.To investigate the relationship between sub-and suprathreshold membrane potential changes of individual neurons in layer 2͞3 and the surrounding network, we combined whole-cell (WC) recordings, VSD imaging, and tetrode recordings for in vivo measurements in rodent barrel cortex. Surprisingly, unlike in the anesthetized cat where spontaneous depolarization enhanced responses (6, 8, 9), here we find that both sensory-evoked postsynaptic potentials (PSPs) and sensory-evoked APs are suppressed by ongoing spontaneous activity. This spontaneous activity occurs as both brief localized depolarizations and propagating waves of glutamatergic excitation in layer 2͞3. MethodsSurgical Procedures. Wistar rats or mice C57BL6 aged P21-P35 were anesthetized with urethane (1.5-2 g/kg), ketamine (100 mg/kg)͞xylazine (20 mg/kg), or halothane (1.5-2%). Paw withdrawal, whisk...

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“…The first of these is the active vasoconstriction of arteries and arterioles through activation of the smooth muscles that line them Hamel, 2006;Iadecola, 2004;Lauritzen, 2005), or the active changes in the diameter of capillaries (Peppiatt et al, 2006). Active vasoconstriction could be induced by the release of neurotransmitters or neuropeptides, and may be associated with centersurround electrophysiological patterns of activity consisting of center excitation and surround inhibition (Cauli et al, 2004;Derdikman et al, 2003;Devor et al, 2007;Faraci and Breese, 1993;Faraci and Sobey, 1998;Hamel, 2006;Takashima et al, 2001). The second possible factor is the simplicity in our VAN model architecture, which does not fully represent the threedimensional (3D) asymmetric structure of a branched vascular network.…”

Section: Center-surround Negativitymentioning

confidence: 99%

A vascular anatomical network model of the spatio-temporal response to brain activation

Boas¹,

Jones²,

Devor³

et al. 2008

NeuroImage

198

240

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Neuronal activity-induced changes in vascular tone and oxygen consumption result in a dynamic evolution of blood flow, volume, and oxygenation. Functional neuroimaging techniques, such as functional magnetic resonance imaging, optical imaging, and PET, provide indirect measures of the neural-induced vascular dynamics driving the blood parameters. Models connecting changes in vascular tone and oxygen consumption to observed changes in the blood parameters are needed to guide more quantitative physiological interpretation of these functional neuroimaging modalities. Effective lumped-parameter vascular balloon and Windkessel models have been developed for this purpose, but the lumping of the complex vascular network into a series of arterioles, capillaries, and venules allows only qualitative interpretation. We have therefore developed a parallel vascular anatomical network (VAN) model based on microscopically measurable properties to improve quantitative interpretation of the vascular response. The model, derived from measured physical properties, predicts baseline blood pressure and oxygen saturation distributions and dynamic responses consistent with literature. Furthermore, the VAN model allows investigation of spatial features of the dynamic vascular and oxygen response to neuronal activity. We find that a passive surround negative vascular response ("negative BOLD") is predicted, but that it underestimates recently observed surround negativity suggesting that additional active surround vasoconstriction is required to explain the experimental data.

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Imaging Spatiotemporal Dynamics of Surround Inhibition in the Barrels Somatosensory Cortex

Cited by 162 publications

References 30 publications

Topological basis for the robust distribution of blood to rodent neocortex

Topological basis for the robust distribution of blood to rodent neocortex

Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex

A vascular anatomical network model of the spatio-temporal response to brain activation

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