Space and Time in the Brain

The science of space and time began with the invention of measuring instruments, which changed these dimensionless concepts into distance and duration with precise units. This process created a special problem for neuroscience. If space and time correspond to their measured variants, we may wonder what space and time mean without such instruments, including for non-human animals who cannot read those instruments. Nonetheless, contemporary neuroscience still lives within the framework of the classical physics view. Our episodic memories are defined as “what happened to me, where, and when.” This is a typical outside-in approach: assume the concepts and search for their homes in the brain. Yet I argue in this chapter that almost everything that we attribute to space and time in the brain can be accomplished by sequential cell assemblies or neuronal trajectories.

Brain Rhythms Provide a Framework for Neural Syntax

Brain oscillations are present in the same form in all mammals and represent a fundamental aspect of neuronal computation, including the generation of movement patterns, speech, and music production. Neuronal oscillators readily entrain each other, making the exchange of messages between brain areas effective. Because all neuronal oscillations are based on inhibition, they can parse and concatenate neuronal messages, a prerequisite for any coding mechanism. This chapter discusses how the hierarchical nature of cross-frequency–coupled rhythms can serve as a scaffold for combining neuronal letters into words and words into sentences, thus providing a syntactic structure for information exchange.

Neuronal Assembly

To effectively send a message, a single neuron must cooperate with its peers. Such cooperation can be achieved by synchronizing their spikes together within the time window limited by the ability of the downstream reader neuron to integrate the incoming signals. Therefore, the cell assembly, defined from the point of view of the reader neuron, can be considered as a unit of neuronal communication, a “neuronal letter.” Acting in assemblies has several advantages. A cooperative assembly partnership tolerates spike rate variation in individual cells effectively because the total excitatory effect of the assembly is what matters to the reader mechanism. Interacting assembly members can compute probabilities rather than convey deterministic information and can robustly tolerate noise even if the individual members respond probabilistically.

Epilogue

The outside is always an inside. —LE CORBUSIER1 It’s what’s inside that counts. —CUBESMART (SUBWAY AD) All enquiry and all learning is but recollection. —SOCRATES IN PLATO’S MENO 1. Le Corbusier (1923). I did not aim to write a perfect book—just a story good enough that the reader can understand my views and challenge them. My goal was not so much to convince but to expose the problems and highlight my offered solutions. Perfection and precise solutions will have to wait for numerous experiments to be performed and reported in detail in scientific journals. I analyzed how an undefined and unagreed-upon terminology, which we inherited from our pre-neuroscience ancestors and never questioned, has become a roadblock to progress. The neuronal mechanisms of invented terms with ill-defined content are hard to discover. Such conceptual confusion is perhaps the primary reason why “my scientist” could not explain to me my pig friend’s cognitive abilities (see the Preface). This message is especially important today, when newly invented terms are again popping up like mushrooms after a rain. I do not insist that my inside-out framework is right or the only way to go, but I hope I presented enough evidence in this book to convince the attentive reader that the outside-in strategy has reached its limits in neuroscience research....

The Brain’s Best Guess

In this final chapter, I propose that behavior-based calibration of perceptions and abstract representations are constrained by a preconfigured brain. The nervous system may have evolved to mimic the statistical probabilities of the physical world and the behavior of already existing species and thus become an efficient predictor of events. Because of their high diversity, neurophysiological and perceptual brain dynamics, both spanning several orders of magnitude, share a common mathematical foundation: the log rule. The tails of these wide and skewed distributions have apparently distinct qualitative features that we describe by discrete words, such as familiar and novel, rigid and plastic, good-enough and precise. Yet every novel situation contains elements of familiarity. Brain correlates of newly acquired experience are not created in the sense of adding new neuronal words to an ever-expanding vocabulary. Instead, the preconfigured brain is a dictionary in which the behavioral significance or meaning of initially nonsense neuronal words is acquired through exploration.

Internally Organized Activity During Offline Brain States

A prime example of internally organized patterns is observed during sleep. The best studied of these is the sharp wave ripple in the hippocampus. Neuronal sequences during ripple events reach back to the past to replay snippets of waking experience at times when the brain is disengaged from the outside world. This process may consolidate episodic memories and stitch together discontiguous experiences, thereby giving rise to creative thoughts. In addition, neuronal assembly sequences during ripples also act as internalized, vicarious, trial-and-error mechanisms that can assist with subconscious optimization of future plans. Because the same neuronal substrate can perform both retrospective and prospective operations, it is not clear whether the traditional separation of postdiction (i.e., memory) from prediction (i.e., planning) is justified.

Everything Is a Relationship

This chapter discusses the hypothesis that the strongly skewed nature of our perceptions and memory result from log-normal distributions of anatomical connectivity at both micro- and mesoscales, synaptic weight distributions, firing rates, and neuronal population activity. Nearly all anatomical and physiological features of the brain are part of a continuous but wide distribution, typically obeying a log-normal form. This organization implies that the interactions that give rise to this distribution involve multiplication or division of random factors, resulting in values that can span several orders of magnitude. Neuronal networks with such broad distributions are needed to maintain stability against competing needs, including wide dynamic range, redundancy, resilience, homeostasis, and plasticity. These features of the brain may explain the Weber-Fechner law: for any sensory modality, perceptual intensity is a logarithmic function of physical intensity. Neuronal systems organized according to log rules form brain networks that can produce good-enough and fast decisions in most situations using only a subset of the brain’s resources.

Internally Organized Cell Assembly Trajectories

Sequences of neuronal patterns are not always imposed on brain circuits in an outside-in manner by the sensory inputs. Internally organized processes can sustain self-organized and coordinated neuronal activity even without external inputs. A prerequisite of cognition is the availability of internally generated neuronal sentences. Self-generated, sequentially evolving activity is the default state of affairs in most neuronal circuits. Neuronal activity moves perpetually, and its trajectory depends only on initial conditions. Large recurrent networks can generate an enormous number of trajectories without prior experience. On the other hand, each is available to be matched by experience to “represent” something useful for the downstream reader mechanisms. The richness of the information depends not on the numbers of generated sequences but on the reader mechanisms. It is typically the reader structure that initiates the transfer of information, coordinating the onset of messages from multiple senders.

Perception from Action

The outside-in framework inevitably poses the question: What comes between perception and action? The homunculus with its decision-making power produces unavoidable logical consequences from the separation of perception from action. I promote the alternative view that things and events in the world can acquire meaning only through brain-initiated actions. In this process, the brain builds a simplified, customized model of the world by encoding the relationships of events to each other. I introduce the concept of “corollary discharge,” the main physiological mechanism that grounds the sensory input to make it an experience. This is a comparator mechanism that allows the brain to examine the relationship between a true change in the sensory input and a change due to self-initiated movement of the sensors.

The Problem

This chapter reviews how empiricist philosophy shaped the dominant outside-in thinking in neuroscience that gave rise to the perception-decision-action framework. In contrast, the inside-out framework takes action as the primary source of knowledge. Action validates the meaning and significance of sensory signals by providing a second opinion. The chapter also compares the relationship between “blank slate” and preconfigured brain models. It describes the brain as a sort of “dictionary” with preexisting internal dynamics and syntactical rules, filled initially with nonsense neuronal words. These nonsense words acquire significance for the animal through exploratory action and represent a distinct event or situation. Preconfigured neuronal networks can generalize and provides fast and “good-enough” solutions under many situations, while detailed and precise computation mobilizes a large fraction of brain resources.