Oscillations in the prefrontal cortex: a gateway to memory and attention

doi:10.1016/j.conb.2011.01.004

Current Opinion in Neurobiology

Volume 21, Issue 3, June 2011, Pages 475-485

https://doi.org/10.1016/j.conb.2011.01.004 Get rights and content

We consider the potential role of oscillations in the prefrontal cortex (PFC) in mediating attention, working memory and memory consolidation. Activity in the theta, beta, and gamma bands is related to communication between PFC and different brain areas. While gamma/beta oscillations mediate bottom-up and top-down interactions between PFC and visual cortices, related to attention, theta rhythms are engaged by hippocampal/PFC interplay. These interactions are dynamic, depending on the nature and relevance of the information currently being processed. The profound modifications of the PFC neuronal network associated with changes in oscillatory coherence are controlled by neuromodulators such as dopamine, which thereby allow or prevent the formation of cell assemblies for information encoding and storage.

Highlights

► Theta and gamma are instrumental for PFC interactions with other brain structures. ► Interneurons control oscillations and coherence across structures. ► Dopamine is important for engaging coherence and neural synchrony.

Introduction

The prefrontal cortex (PFC) sits at the top of the sensorimotor cortical hierarchy, and has a key role for the representation, planning and execution of actions at the highest level of cognitive ability [1, 2].

The function of PFC is multifaceted [3, 4], with three prominent aspects, first, its role in working memory, the temporary storage of information as a buffer for internal manipulation ([3], see e.g. [5]). Second, it is involved in attentional processes [6, 7••]. Third, it has an important role in long-term memory and memory consolidation (see e.g. [8••, 9, 10, 11, 12]).

These apparently heterogeneous prefrontal tasks have two common themes: orchestration of neural activity all over the brain, through the PFC connections with cortical, subcortical and neuromodulatory structures and selecting and retaining relevant information.

Here, we review recent data on how neural oscillations in different frequency ranges, in particular theta (6–10 Hz), and gamma (30–120 Hz) may contribute to shape the temporal structure of neural activity in PFC and act as carriers for communication between the PFC and the rest of the brain, serving multiple aspects of prefrontal function. We also discuss how the interplay of excitatory and inhibitory cells generates and controls oscillations, and how neuromodulators, especially dopamine, may modulate the level of neural activity, oscillations and synchronization in PFC, thereby providing a possible mechanism for mediating interareal communication and information selection and processing.

Section snippets

Gamma oscillations in PFC and attention

The overwhelming influx of sensory information to the brain needs to be filtered in order to select the information critical to survival. This requires a constant dialog between sensory areas that represent information and frontal areas that set goals and thus determine what is relevant. In primates, fast oscillations (beta, 15–30 Hz; gamma) are hypothesized to play an important role in the attention processes underlying stimulus selection by enhancing the neuronal representation of attended

Oscillation in the PFC in the theta band: learning and memory

Theta (5–10 Hz) oscillations are observed in the PFC [8••, 47, 48••, 49••, 50, 51], both in the local field potential and in the spiking of single neurons. Theta is a very important component of the interaction between the prefrontal cortex and the hippocampus, where theta is predominant during active behavior [52]. Theta oscillations are also the carrier of functional networks linking the hippocampus with, for example, the striatum [53] and the amygdala [54].

In rodents, it has been shown that

Neuromodulation, dopamine and latent theta oscillators

In the study by Benchenane et al. [8^••], theta coherence and cell assembly synchronization emerge when a prediction can be made about the upcoming reward and the animal decides which arm to enter. Furthermore, coherence also correlates with the animal performance level, which is arguably connected to the reliability of the reward prediction. Reward expectation also affects the theta phase locking of orbitofrontal (a PFC subdivision) neurons [76]. In the brain, reward expectation signals are

Conclusions

PFC is involved in multiple functional networks, for example those connecting it to the visual cortex to subserve attention, and to the hippocampus supporting memory storage and consolidation. The former seems to rely mostly on gamma and beta oscillations, with beta being more relevant for long-range synchronization involving long transmission delays [87] and gamma being more evident in the communication of close-by areas (but see [7^••]). Communication with the hippocampus appears to depend

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

References (91)

E. Koechlin et al.
An information theoretical approach to prefrontal executive function
Trends Cogn Sci
(2007)
J.M. Fuster
The prefrontal cortex – an update: time is of the essence
Neuron
(2001)
R.C. O’Reilly
The What and How of prefrontal cortical organization
Trends Neurosci
(2010)
T. Maviel et al.
Sites of neocortical reorganization critical for remote spatial memory
Science
(2004)
P. Fries et al.
Modulation of oscillatory neuronal synchronization by selective visual attention
Science
(2001)
P. Fries et al.
The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4
J Neurosci
(2008)
S. Ray et al.
Differences in gamma frequencies across visual cortex restrict their possible use in computation
Neuron
(2010)
E. Salinas et al.
Correlated neuronal activity and the flow of neural information
Nat Rev Neurosci
(2001)
P. Tiesinga et al.
Cortical enlightenment: are attentional gamma oscillations driven by ING or PING?
Neuron
(2009)
M. Bartos et al.
Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks
Nat Rev Neurosci
(2007)

V.S. Sohal et al.

Parvalbumin neurons and gamma rhythms enhance cortical circuit performance

Nature

(2009)

A. Belitski et al.

Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information

J Neurosci

(2008)

T.J. Buschman et al.

Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices

Science

(2007)

D. McLelland et al.

Neuronal oscillations and the rate-to-phase transform: mechanism, model and mutual information

J Physiol

(2009)

D.O. Hebb

The Organization of Behavior

(1949)

U. Rutishauser et al.

Human memory strength is predicted by theta-frequency phase-locking of single neurons

Nature

(2010)

C.A. Chapman et al.

Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare

J Neurophysiol

(1999)

C.I. Buia et al.

Role of interneuron diversity in the cortical microcircuit for attention

J Neurophysiol

(2008)

M. van Wingerden et al.

Theta-band phase locking of orbitofrontal neurons during reward expectancy

J Neurosci

(2010)

P.L. Tierney et al.

Dopamine modulates temporal dynamics of feedforward inhibition in rat prefrontal cortex in vivo

Cereb Cortex

(2008)

M.E. Hasselmo

Neuromodulation and cortical function: modeling the physiological basis of behavior

Behav Brain Res

(1995)

E.K. Miller et al.

An integrative theory of prefrontal cortex function

Annu Rev Neurosci

(2001)

S. Funahashi et al.

Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex

J Neurophysiol

(1989)

R. Desimone et al.

Neural mechanisms of selective visual attention

Annu Rev Neurosci

(1995)

G.G. Gregoriou et al.

High-frequency, long-range coupling between prefrontal and visual cortex during attention

Science

(2009)

K. Benchenane et al.

Coherent theta oscillations and reorganization of spike timing in the hippocampal–prefrontal network upon learning

Neuron

(2010)

P.W. Frankland et al.

The organization of recent and remote memories

Nat Rev Neurosci

(2005)

A. Takashima et al.

Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study

Proc Natl Acad Sci U S A

(2006)

K. Takehara-Nishiuchi et al.

Spontaneous changes of neocortical code for associative memory during consolidation

Science

(2008)

T. Womelsdorf et al.

The role of neuronal synchronization in selective attention

Curr Opin Neurobiol

(2007)

B. Noudoost et al.

Top-down control of visual attention

Curr Opin Neurobiol

(2010)

M. Chalk et al.

Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1

Neuron

(2010)

L.L. Colgin et al.

Frequency of gamma oscillations routes flow of information in the hippocampus

Nature

(2009)

P. Fries

Neuronal gamma-band synchronization as a fundamental process in cortical computation

Annu Rev Neurosci

(2009)

P.H. Tiesinga et al.

Inhibitory synchrony as a mechanism for attentional gain modulation

J Physiol Paris

(2004)

P. Fries

A mechanism for cognitive dynamics: neuronal communication through neuronal coherence

Trends Cogn Sci

(2005)

P.H. Tiesinga et al.

Mechanisms for phase shifting in cortical networks and their role in communication through coherence

Front Hum Neurosci

(2010)

J.A. Cardin et al.

Driving fast-spiking cells induces gamma rhythm and controls sensory responses

Nature

(2009)

M.A. Whittington et al.

Inhibition-based rhythms: experimental and mathematical observations on network dynamics

Int J Psychophysiol

(2000)

T. Womelsdorf et al.

Modulation of neuronal interactions through neuronal synchronization

Science

(2007)

A. Buehlmann et al.

Optimal information transfer in the cortex through synchronization

PLoS Comput Biol

(2010)

T. Akam et al.

Oscillations and filtering networks support flexible routing of information

Neuron

(2010)

A. Mazzoni et al.

Encoding of naturalistic stimuli by local field potential spectra in networks of excitatory and inhibitory neurons

PLoS Comput Biol

(2008)

J.A. White et al.

Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons

J Comput Neurosci

(1998)

C. Börgers et al.

Effects of noisy drive on rhythms in networks of excitatory and inhibitory neurons

Neural Comput

(2005)

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Oscillations in the prefrontal cortex: a gateway to memory and attention

Highlights

Introduction

Section snippets

Gamma oscillations in PFC and attention

Oscillation in the PFC in the theta band: learning and memory

Neuromodulation, dopamine and latent theta oscillators

Conclusions

References and recommended reading

Trends Cogn Sci

Neuron

Trends Neurosci

Science

Science

J Neurosci

Neuron

Nat Rev Neurosci

Neuron

Nat Rev Neurosci

Nature

J Neurosci

Science

J Physiol

Nature

J Neurophysiol

J Neurophysiol

J Neurosci

Cereb Cortex

Behav Brain Res

An integrative theory of prefrontal cortex function

Annu Rev Neurosci

Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex

J Neurophysiol

Neural mechanisms of selective visual attention

Annu Rev Neurosci

High-frequency, long-range coupling between prefrontal and visual cortex during attention

Science

Coherent theta oscillations and reorganization of spike timing in the hippocampal–prefrontal network upon learning

Neuron

The organization of recent and remote memories

Nat Rev Neurosci

Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study

Proc Natl Acad Sci U S A

Spontaneous changes of neocortical code for associative memory during consolidation

Science

The role of neuronal synchronization in selective attention

Curr Opin Neurobiol

Top-down control of visual attention

Curr Opin Neurobiol

Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1

Neuron

Frequency of gamma oscillations routes flow of information in the hippocampus

Nature

Neuronal gamma-band synchronization as a fundamental process in cortical computation

Annu Rev Neurosci

Inhibitory synchrony as a mechanism for attentional gain modulation

J Physiol Paris

A mechanism for cognitive dynamics: neuronal communication through neuronal coherence

Trends Cogn Sci

Mechanisms for phase shifting in cortical networks and their role in communication through coherence

Front Hum Neurosci

Driving fast-spiking cells induces gamma rhythm and controls sensory responses

Nature

Inhibition-based rhythms: experimental and mathematical observations on network dynamics

Int J Psychophysiol

Modulation of neuronal interactions through neuronal synchronization

Science

Optimal information transfer in the cortex through synchronization

PLoS Comput Biol

Oscillations and filtering networks support flexible routing of information

Neuron

Encoding of naturalistic stimuli by local field potential spectra in networks of excitatory and inhibitory neurons

PLoS Comput Biol

Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons

J Comput Neurosci

Effects of noisy drive on rhythms in networks of excitatory and inhibitory neurons

Neural Comput