Explaining Conscious Memory Formation and Retrieval

It's all about the timing of brain electrical activity.

Posted Mar 21, 2020

When you memorize something, the brain creates a nerve-impulse code to create a representation of the information represented in the brain, and this code can get stored in memory. Upon retrieval, the code is replayed, and thus what the code represents becomes consciously available again as a simulation. At least that’s the theory. Until now, the evidence for this explanation has been derived mostly from rodents. But now rather direct evidence is available from humans.

In one new study, human subjects created memory associations between word pairs, while experimenters simultaneously recorded single-neuron impulses and their associated field potentials from an implanted microelectrode array in the medial temporal cortex, which is known to participate in memory formation. The EEG was also recorded from subdural electrodes implanted over the temporal cortex immediately above the microelectrode array. This allowed simultaneous observation of the local nerve impulse discharges, their associated local field potentials, and the EEG during memory formation and retrieval after a brief distraction period.

Recordings revealed the well-known relationship that EEG signals often have superimposed low-voltage high-frequency waves, which are called ripples. As expected, the ripples appeared at the same time as the impulse discharges from the microelectrodes, indicating that the impulses actually cause the small field potential changes of ripples.

 Saimee et al., used with permission
Ripple voltages nested within large slow voltage waves.
Source: Saimee et al., used with permission

In the top signal, we have the sum of fast and slow oscillations, where the power of fast oscillation's envelope changes with the phase of the slower oscillation. The bottom signal shows only the filtered fast oscillation and the variation in its power. As it is obvious from a comparison of two signals, the fast rhythm's power is always maximum at a certain coupled phase of slower oscillation (From Samiee et al.).

In the experiment, impulse burst clusters occurred throughout the presentation of word pairs while subjects were encoding the pairs. Trial-specific spike sequences observed during encoding were replayed during correct recall. As expected, ripples during recall appeared at the same time as the impulse sequences.

Not mentioned by the authors is that their findings have implications for neural correlates of consciousness. After all, forming the word-pair associations was a conscious operation. In the field of consciousness research, neural correlates are clearly evident in the EEG in that the frequency of voltage shifts predictably as the brain progresses from large slow waves during anesthesia or sleep to increasingly faster and smaller waves during alert arousal. Relatively high frequencies (40-200 waves per second) appear more prominently when the brain is working on difficult tasks. Moreover, hard tasks are associated with more phase-locking of the EEG oscillations at different locations of the cortex.

Conscious perceptions seem to involve short- and long-range oscillations in the vertically oriented network columns in the cortex. Each column contains a local network that processes input locally in oscillatory activity that is gated at certain frequencies by inhibitory neurons in the circuit.  

At the same time, local oscillations from large pyramidal cell firings spread to distant columns both within and between the cortical hemispheres. The frequencies of this long-range activity may be slower because of the longer impulse conduction and synaptic delays. Collectively, local and distant networks interact and may likely be the basis for consciousness. The electrographic correlate is that of fast frequencies from local processing being nested within more globally generated slow frequencies. The timing phase relationships would clearly influence how much integration of local and distant processing occurs and the likelihood that the processing could be consciously perceived.

Many experiments have shown that selective attention is needed for conscious perception. Such attention activates local processing (and ripples in the local field potential). Bear in mind, however, that the ripples are not the source of processing but rather an associated manifestation of the processing that is actually occurring via the impulse timing in the local circuitry.

Two basic kinds of coupling can be seen in brainwave activity: 1) the phase of the slower frequency modulates the faster frequency, and 2) the phase coupling between two overlapping frequencies occurs when one frequency is a harmonic multiple of the other.

Conscious processing seems to be crucially dependent on the cross-frequency coherence of neural activity that can be seen at the local circuit level in multiple local sites of neocortex, hippocampus, and basal ganglia. There are different varieties of cross-frequency coupling (phase-phase, amplitude-amplitude, and phase-amplitude coupling), each of which may reflect distinctive processing. Such coherence differs across brain areas in a task-relevant manner, changes quickly in response to sensory, motor, and cognitive events, and correlates with performance in learning tasks. Moreover, cross-frequency coherence increases with level of task demand. For example, continuous EEG recordings obtained during an arithmetic task, rest and breath focus revealed that cross-frequency alpha and theta peak-frequency coherence is significantly higher when cognitive demands increased (Rodriguez-Larios and Alaerts, (2019). What is likely to remain enigmatic is how such cross-frequency coupling yields a conscious perception.

The most significant neural correlation of consciousness may prove to be time locking of nested oscillation of different frequencies whose underlying impulse patterns carry different aspects of information. The time locking of nested high- and low-frequency activity likely increases information throughput in the local circuits participating in selective attention, occludes noisy disruption from other inputs, and improves the signal-to-noise ratio of neural activity that is processing the target of attention. Parsimonious as this view might be, it still does not fully explain how a conscious perception emerges.


Rodriguez_Larios, Julio and Alaerts, Kaat (2019). Tracking transient changes in the neural frequency architecture: harmonic relations between theta and alpha peaks facilitate cognitive performance. J. Neurosci. 7 August, 39 (32) 6291-6298; DOI: https://doi.org/10.1523/JNEUROSCI.2919-18.2019

Samiee, Sohelila et al. (2019) Phase-amplitude coupling. Nov. https://neuroimage.usc.edu/brainstorm/Tutorials/TutPac

Vaz, Alex P. et al. (2020). Replay of cortical spiking sequences during human memory retrieval. Science. 367,1131-1134.