Gamma Band Gamma Band OscillationOscillation

The Binding Problem & Binding by The Binding Problem & Binding by SynchronizationSynchronization

OutlineOutline

What are Gamma Oscillations?What are Gamma Oscillations? Where are they found?Where are they found? What is the “Binding Problem”?What is the “Binding Problem”? Hierarchal ModelHierarchal Model The Temporal Binding Hypothesis and Binding by The Temporal Binding Hypothesis and Binding by

SynchronySynchrony Evidence and the role of Gamma OscillationsEvidence and the role of Gamma Oscillations Criticisms or the Temporal Binding HypothesisCriticisms or the Temporal Binding Hypothesis Future Research and DirectionsFuture Research and Directions

SourcesSources Rhythms of the Brain – Rhythms of the Brain – György BuzsákiGyörgy Buzsáki Synchrony Unbound: A Critical Evaluation of the Temporal Binding Hypothesis – Synchrony Unbound: A Critical Evaluation of the Temporal Binding Hypothesis –

Shadlen, M., & Movshon, J.A.Shadlen, M., & Movshon, J.A. Neural synchrony in cortical networks: history, concept and current status - Uhlhass et Uhlhass et

al. (2009) al. (2009)

Gamma OscillationsGamma Oscillations

The fastest frequency band of neural oscillations The fastest frequency band of neural oscillations

≈ ≈ 20 – 100 Hz (typically 40-60 Hz) 20 – 100 Hz (typically 40-60 Hz) ““..[Oscillations are] not independent events that ..[Oscillations are] not independent events that

impose timing on neuronal spiking but rather are a impose timing on neuronal spiking but rather are a reflection of reflection of self-organized interactionsself-organized interactions of those of those same neurons that detect, transfer, and store same neurons that detect, transfer, and store information”. (Buzsáki, p 259) information”. (Buzsáki, p 259)

Being fast and having a small amplitude, Gamma Being fast and having a small amplitude, Gamma band oscillations were hard to detect in early cell band oscillations were hard to detect in early cell recordingrecording

Where do we find Gamma Where do we find Gamma Oscillations?Oscillations? Gamma frequency Gamma frequency

oscillations are present oscillations are present during waking, slow-wave during waking, slow-wave and REM sleep.and REM sleep.

They are intrinsic to the They are intrinsic to the neo-cortex, and heavily neo-cortex, and heavily rely on GABA-a rely on GABA-a receptors, as it mediates receptors, as it mediates the time constant of the the time constant of the decay of IPSPs, which decay of IPSPs, which varies from 10 – 25 ms varies from 10 – 25 ms (40 – 100 Hz)(40 – 100 Hz)

““Most characteristic field Most characteristic field pattern of the waking, pattern of the waking, activated neocortex..” activated neocortex..” (Buzsáki, p.259)(Buzsáki, p.259)

The Binding ProblemThe Binding Problem

The problem can be found in both neuroscience and The problem can be found in both neuroscience and philosophy, however they are unique in both cases.philosophy, however they are unique in both cases.

In neuroscience, the question is; how higher-order In neuroscience, the question is; how higher-order neural structures are able to segregate and integrate neural structures are able to segregate and integrate the proper inputs, both from sensory organs and the proper inputs, both from sensory organs and internal computations? internal computations?

In areas such as V1 this is partly accounted for by In areas such as V1 this is partly accounted for by the discovery of cortical columns consisting of the discovery of cortical columns consisting of simple, complex and hypercomplex cells, which are simple, complex and hypercomplex cells, which are attuned to certain stimuli. attuned to certain stimuli.

However, there remains the question of how we are However, there remains the question of how we are able to perceive as unified objects, stimuli in a able to perceive as unified objects, stimuli in a robust manner; regardless of out point of view, size robust manner; regardless of out point of view, size and lighting conditions. (Buzsáki, p 232)and lighting conditions. (Buzsáki, p 232) Ex. Our ability to reliably recognize all dogs. Ex. Our ability to reliably recognize all dogs.

The Binding ProblemThe Binding Problem Our brains are able to take Our brains are able to take

different features such as “…different features such as “…colour, texture, distance, colour, texture, distance, spatial position and smell spatial position and smell [which are] processed in [which are] processed in separate parts of the cortex separate parts of the cortex by different sets of neurons by different sets of neurons [and] are bound into a [and] are bound into a complex representation in a complex representation in a matter of 200 milliseconds…” matter of 200 milliseconds…” (Buzsáki, p260)(Buzsáki, p260)

This type of mental This type of mental reconstruction has been reconstruction has been largely documented by largely documented by Gestaltian psychologists; Gestaltian psychologists; showing that human regularly, showing that human regularly, and systematically impose and systematically impose top-down rules on visual top-down rules on visual stimuli. stimuli.

Hierarchical ModelHierarchical Model

An early solution to the Binding problem; a An early solution to the Binding problem; a feed-forward design where lower level feed-forward design where lower level information is projected to higher level neural information is projected to higher level neural structures, and based on which structures structures, and based on which structures are activated, .a “Gnostic” cardinal cell are activated, .a “Gnostic” cardinal cell activates. (also called a “grandmother” cell)activates. (also called a “grandmother” cell)

This cell represents the object or concept This cell represents the object or concept which fed the sensory input; if it is active which fed the sensory input; if it is active then the mental representation for a then the mental representation for a particular stimulus is activated, if it is not particular stimulus is activated, if it is not activated, then there is no internal activated, then there is no internal representation. representation.

There has to be a Gnostic cell for every There has to be a Gnostic cell for every object, concept or referent in the object, concept or referent in the

environment. environment. This is problematic because the model This is problematic because the model

focuses on the role of excitatory cells, while focuses on the role of excitatory cells, while eliminating the need for inhibitory eliminating the need for inhibitory interneurons.interneurons.

Also, there just aren’t enough neurons for Also, there just aren’t enough neurons for there to be dedicated high-order structures there to be dedicated high-order structures for each concept or object. “Combinatorial for each concept or object. “Combinatorial Explosion”Explosion”

Hierarchical ModelHierarchical Model

““Because the number of neurons needed grows exponentially with the Because the number of neurons needed grows exponentially with the number of unique objects represented by their numerous features, the number of unique objects represented by their numerous features, the brain, so the story goes, quickly runs out of neurons”. (Buzsáki p. 236) – brain, so the story goes, quickly runs out of neurons”. (Buzsáki p. 236) – Combinatorial ExplosionCombinatorial Explosion

The Hierarchical Model also does not specify the location or spatial The Hierarchical Model also does not specify the location or spatial relationship of the Gnostic units. relationship of the Gnostic units.

If they are clustered in particular areas, then they would be easily If they are clustered in particular areas, then they would be easily susceptible to damage in case of injury or brain damage. However susceptible to damage in case of injury or brain damage. However this does not appear to be the case in patients with cortical column this does not appear to be the case in patients with cortical column damage.damage.

If they are widely distributed, then there remains the problem of how If they are widely distributed, then there remains the problem of how they communicate; and what kind of specialized connectivity they they communicate; and what kind of specialized connectivity they would requirewould require. .

Finally, this model lacks a temporal scale, and it would therefore still need Finally, this model lacks a temporal scale, and it would therefore still need to be explained how it could effectively be used in real-world time and to be explained how it could effectively be used in real-world time and environments. (Buzsáki p, 237)environments. (Buzsáki p, 237)

The Temporal Binding The Temporal Binding HypothesisHypothesis A solution to the Binding problem requires an explanation A solution to the Binding problem requires an explanation

of how the various inputs and neural computations are of how the various inputs and neural computations are differentiated so that the right bits of information can be differentiated so that the right bits of information can be compared and integrated.compared and integrated.

For this, “…it is necessary to “tag” each visual neuron to For this, “…it is necessary to “tag” each visual neuron to signify the object to which its activity relates” (Shadlen & signify the object to which its activity relates” (Shadlen & Movshon)Movshon)

In the Temporal Binding Hypothesis, this tag is indicated In the Temporal Binding Hypothesis, this tag is indicated by synchronous neural spiking.by synchronous neural spiking.

This offers an endless capacity for coding combinations.This offers an endless capacity for coding combinations. Synchronous spiking also allows for cross modal and long Synchronous spiking also allows for cross modal and long

range communication.range communication.

The Temporal Binding The Temporal Binding Hypothesis (examples)Hypothesis (examples)

In Figure A., focusing on the In Figure A., focusing on the blue lines; in order for us to blue lines; in order for us to accurately perceive that there accurately perceive that there are two separate lines, and the are two separate lines, and the proper configuration, we need to proper configuration, we need to be able to label point be able to label point yy and point and point zz in the retina and subsequent in the retina and subsequent retinotopic visual areas so that retinotopic visual areas so that higher-order areas properly higher-order areas properly segregate the stimulus, and segregate the stimulus, and therefore allowing us to properly therefore allowing us to properly perceive the image. perceive the image.

In Figure B. however, the same In Figure B. however, the same two points in the field of vision two points in the field of vision need to be tagged as bound need to be tagged as bound component in the visual scene, component in the visual scene, in order for accurate perception.in order for accurate perception.

It is believed that the manner in It is believed that the manner in which this labelling occurs is which this labelling occurs is through neuronal oscillations. through neuronal oscillations.

Evidence Evidence – – From: Gray and Singer (1989); as shown in Buzsáki (2006)From: Gray and Singer (1989); as shown in Buzsáki (2006)

Singer and Gray recorded both multi-unit activity and local field potentials Singer and Gray recorded both multi-unit activity and local field potentials (LFP) from single electrodes placed in the Primary visual cortex of (LFP) from single electrodes placed in the Primary visual cortex of anesthetised and paralyzed cats.anesthetised and paralyzed cats.

Using a correlational analysis of cell activity and Fourier analysis, they Using a correlational analysis of cell activity and Fourier analysis, they noticed that a significant proportion of the recordings showed Gamma noticed that a significant proportion of the recordings showed Gamma frequency oscillations. (30-60 Hz)frequency oscillations. (30-60 Hz)

This oscillatory response was induced by visual stimulus, consisting of This oscillatory response was induced by visual stimulus, consisting of moving bars.moving bars.

The cell activity was phase-locked to the trough of the field oscillations.The cell activity was phase-locked to the trough of the field oscillations. ““These findings provided conclusive evidence that the oscillatory These findings provided conclusive evidence that the oscillatory

ensemble events emerged locally… [and] were not directly related to the ensemble events emerged locally… [and] were not directly related to the stimulus but stimulus but were added on by the brainwere added on by the brain.” (Buzsáki, p. 240).” (Buzsáki, p. 240)

Synchrony between various locations occurred Synchrony between various locations occurred only only when neurons at when neurons at those locations responded to related visual features of the object. those locations responded to related visual features of the object. Furthermore, the determining factor of the “vigour of synchrony” was the Furthermore, the determining factor of the “vigour of synchrony” was the response features of the neurons.response features of the neurons.

During stimulus-induced transient oscillations, neurons several millimetres During stimulus-induced transient oscillations, neurons several millimetres apart, and even contralateral to each other synchronized. apart, and even contralateral to each other synchronized.

Evidence and the Role of Evidence and the Role of Gamma OscillationsGamma Oscillations In experiments recording multiple neurons in two separate In experiments recording multiple neurons in two separate

recording sites in the ‘motion-sensitive’ MT area of recording sites in the ‘motion-sensitive’ MT area of waking waking monkeys, experimenters stimulated both sites simultaneously, monkeys, experimenters stimulated both sites simultaneously, using 2 bars moving in the preferred directions of the neurons.using 2 bars moving in the preferred directions of the neurons.

In these trials, there was rarely oscillatory coupling!In these trials, there was rarely oscillatory coupling! Experimenters then substituted the stimuli with a single bar, Experimenters then substituted the stimuli with a single bar,

which activated both neuronal sites.which activated both neuronal sites. In these trials, there was In these trials, there was robust synchronyrobust synchrony!!

Therefore the oscillatory synchrony was produced not by the Therefore the oscillatory synchrony was produced not by the simultaneous excitations of both recording sites, but induced by simultaneous excitations of both recording sites, but induced by the coherence of the stimulus.the coherence of the stimulus.

Gamma-frequency power has been shown in motor areas during, Gamma-frequency power has been shown in motor areas during, and more typically prior to voluntary movement.and more typically prior to voluntary movement.

Gamma oscillations are commonly induced between 150-300 ms Gamma oscillations are commonly induced between 150-300 ms after stimulus onset, “approximately at the time when stimulus after stimulus onset, “approximately at the time when stimulus acquire meaning” (Buzsáki, p.244)acquire meaning” (Buzsáki, p.244)

Binding by Synchrony -Binding by Synchrony -Gamma Oscillations Gamma Oscillations If Gamma oscillations are to tag certain signals, then it should If Gamma oscillations are to tag certain signals, then it should

follow that they are only found in selective brain areas, and are follow that they are only found in selective brain areas, and are not entirely identical; in fact, Intracranial and Subdural not entirely identical; in fact, Intracranial and Subdural recordings in human corroborate this prediction. recordings in human corroborate this prediction.

““Recording sites as close as 3-4 millimetres from each other in the Recording sites as close as 3-4 millimetres from each other in the visual cortex yielded quite different amplitudes of gamma visual cortex yielded quite different amplitudes of gamma oscillations”. (Buzsáki, p.245)oscillations”. (Buzsáki, p.245)

Experiments in patients with many subdural electrodes showed Experiments in patients with many subdural electrodes showed that gamma power increased linearly with memory load (when that gamma power increased linearly with memory load (when memorizing strings of syllables), especially above the prefrontal memorizing strings of syllables), especially above the prefrontal cortex; with power levels remaining high until retention was lost cortex; with power levels remaining high until retention was lost and working memory was relaxed. and working memory was relaxed.

There is increasing evidence such as this, suggesting that; “…There is increasing evidence such as this, suggesting that; “…gamma oscillations are used in the brain for temporally gamma oscillations are used in the brain for temporally segmenting representations of different items”. (Buzsáki)segmenting representations of different items”. (Buzsáki)

Criticism of the Temporal Criticism of the Temporal Binding HypothesisBinding Hypothesis Michael N. Shadlen and J. Anthony Movshon, in their 1999 Review Michael N. Shadlen and J. Anthony Movshon, in their 1999 Review

entitled entitled “Synchrony Unbound: A Critical Evaluation of the Temporal “Synchrony Unbound: A Critical Evaluation of the Temporal Binding Hypothesis”Binding Hypothesis” brought up roughly a dozen critical concerns brought up roughly a dozen critical concerns about the reality of Oscillatory Binding.about the reality of Oscillatory Binding.

1.1. The hypothesis is not a theory about how binding is The hypothesis is not a theory about how binding is computedcomputed; it is a theory ; it is a theory only of how binding is only of how binding is signalled.signalled.

2.2. How does the visual system decide which elements are part of single objects How does the visual system decide which elements are part of single objects and which belong to different objects?and which belong to different objects?

3.3. Full image segmentation (and recognition) Full image segmentation (and recognition) probablyprobably requires even higher- requires even higher-level analyses, including the explicit inclusion of information from memory level analyses, including the explicit inclusion of information from memory about the nature and structure of previously viewed objects and scenes.about the nature and structure of previously viewed objects and scenes.

4.4. If binding is not computed in the primary visual cortex [as this level of If binding is not computed in the primary visual cortex [as this level of computation focuses on extremely particular features (i.e. edge/contrast computation focuses on extremely particular features (i.e. edge/contrast detection and orientation) at a micro level] why is synchrony to be expected detection and orientation) at a micro level] why is synchrony to be expected there?there?

5.5. Proponents have stated that “synchronized signals would be particularly Proponents have stated that “synchronized signals would be particularly effective in activating post-synaptic neurons that operate as effective in activating post-synaptic neurons that operate as coincidence coincidence detectorsdetectors. But, how would these . But, how would these coincidence detectors coincidence detectors differ from Gnostic differ from Gnostic cells?cells?

6.6. Oscillations are observed in the cortex which have nothing to do with Oscillations are observed in the cortex which have nothing to do with perceptual binding, as well, there will always be asynchronous “renegade” perceptual binding, as well, there will always be asynchronous “renegade” spiking; How do the postsynaptic neurons distinguish which is “special” spiking; How do the postsynaptic neurons distinguish which is “special” synchrony that is suppose to convey additional information?synchrony that is suppose to convey additional information?

7.7. How is the brain supposed to distinguish the temporal modulation due to How is the brain supposed to distinguish the temporal modulation due to visual input from the temporal modulation produced intrinsically?visual input from the temporal modulation produced intrinsically?

Criticism of the Temporal Criticism of the Temporal Binding HypothesisBinding Hypothesis

8.8. Temporally precise visual activity is Temporally precise visual activity is sufficientsufficient for binding, but it is for binding, but it is not not necessarynecessary for binding and its disruption does not affect for binding and its disruption does not affect binding elicited by other cues. (In the segmentation of visual binding elicited by other cues. (In the segmentation of visual stimuli.)stimuli.)

9.9. The prevalence of gamma oscillatory responses varies widely The prevalence of gamma oscillatory responses varies widely from laboratory to laboratory, for unknown reason.from laboratory to laboratory, for unknown reason.

1.1. While Singer, Eckhorn and Livingstone find oscillatory While Singer, Eckhorn and Livingstone find oscillatory responses in about half their recordings, most others find responses in about half their recordings, most others find their prevalence to be in about 2%-5% of recording sites.their prevalence to be in about 2%-5% of recording sites.

10.10. Initial experiments, from which the theory was developed were Initial experiments, from which the theory was developed were conducted on anesthetised animals. How much did this affect the conducted on anesthetised animals. How much did this affect the results?results?

11.11. Since no perceptual judgements were made during the Since no perceptual judgements were made during the experiments, evidence that the chosen stimulus configurations experiments, evidence that the chosen stimulus configurations actually promoted perceptual binding was circumstantial. The actually promoted perceptual binding was circumstantial. The experiments typically used stimuli that promoted binding-like experiments typically used stimuli that promoted binding-like effects in human observers, but did not establish that effects in human observers, but did not establish that experimental animals perceived the stimuli in the same way.experimental animals perceived the stimuli in the same way.

So what does this mean for the Temporal Binding So what does this mean for the Temporal Binding Hypothesis?Hypothesis?

Future ResearchFuture Research

Research of the Temporal Binding Hypothesis has suggested that there Research of the Temporal Binding Hypothesis has suggested that there may well be a solution to the Binding Problem.may well be a solution to the Binding Problem.

However, experimental results are fairly heterogeneous, and many However, experimental results are fairly heterogeneous, and many researchers fail to observe the type of gamma band oscillations which are researchers fail to observe the type of gamma band oscillations which are implicated in perceptual, and conceptual binding, as well as those which implicated in perceptual, and conceptual binding, as well as those which may be implicated in memory and consciousness.may be implicated in memory and consciousness.

Shadlen and Movshon bring up many questions which still need to be Shadlen and Movshon bring up many questions which still need to be address in order for Binding by Synchrony to become a complete theory.address in order for Binding by Synchrony to become a complete theory.

More experimentation needs to be done in order to answer some of these More experimentation needs to be done in order to answer some of these questions; however finer grained analysis of local and long range questions; however finer grained analysis of local and long range oscillations are hard to record. Higher spatial and even temporal oscillations are hard to record. Higher spatial and even temporal resolution is required in order to give researchers a better picture of the resolution is required in order to give researchers a better picture of the behaviour of gamma oscillations, and its role in Mental Binding.behaviour of gamma oscillations, and its role in Mental Binding.

Regardless of whether gamma band oscillations are relevant in perceptual Regardless of whether gamma band oscillations are relevant in perceptual binding, the question still needs to be addressed; Whether gamma binding, the question still needs to be addressed; Whether gamma oscillations play a role in our brain function, or whether they are merely an oscillations play a role in our brain function, or whether they are merely an epiphenomenon, a by-product of the actual causal agents of our central epiphenomenon, a by-product of the actual causal agents of our central nervous system. nervous system.