Summing Up

A major challenge in neuroscience today is to decipher the operating principle of the brain and the rest of the nervous system in the same straightforward way that biologists have come to understand the functions of other organs and organ systems (e.g., the cardiovascular system, the digestive system, and so on). The argument here has been that the function of nervous systems is to make, maintain, and modify neural associations that ultimately promote survival and reproduction in a world that sensory systems can’t apprehend. In this way, we and other animals can link the subjective domain of perception to successful behavior without ever recovering the properties of the world. Neural function on a wholly empirical basis may be the key to understanding how brains operate.

The Problem

Although understanding neural functions has progressed at a remarkable pace in recent decades, a fundamental question remains: How does the nervous system relate the objective world to the subjective domain of perception? Everyday experience implies that the neural connections on which we and other animals depend link physical parameters in the environment with useful responses. But that interpretation won't work: biological sensory systems cannot measure the physical world. Whereas something is linking sensory inputs to useful responses, it is not the physical world that instruments measure. How, then, have we animals met this challenge, and what is it that we end up perceiving? The purpose of this chapter is to suggest how nervous systems have evolved to deal with the inability to convey the objective properties of the real world.

The Organization of Nervous Systems

Nervous systems employ some or all of the senses to convert energy at the level of receptor cells into neural information. This conversion generates electrochemical signals carried centrally that, via a series of additional neurons, determine behavior. The most obvious behaviors are those mediated by skeletal muscles, cardiac muscles, smooth muscles, and glands. But motor responses are members of a longer list that includes attention, perception, emotion, memory, thought, motivation, and others. How to describe these additional “systems,” and how to decipher what the relevant circuits do and how they do it, are unanswered questions. This chapter describes the main features of neural processing, asking whether the principle of neural function is simply to make associations that lead to useful behaviors.

Organisms With Nervous Systems

Definitions of the term “animals” in dictionaries and textbooks are surprisingly vague. The characteristics usually mentioned are eukaryotic, multicellular, heterotrophic, sexually reproducing, and capable of rapid and independent movement. But some or all of these properties are characteristic of many organisms in the other kingdoms of life on Earth. In fact, the major distinguishing feature of animals in most cases is the presence of a nervous system. But if nervous systems are indeed one of the main attributes that distinguish organisms in the animal kingdom, what exactly are nervous systems and what advantages do they bring? Without at least some provisional answers, seeking the operating principle of neural systems would be futile.

Evidence from Audition

The reason for using vision as an example in the previous three chapters is that more is known about the human visual system and visual psychophysics than about other neural systems. But this choice begs the question of whether other systems corroborate the evidence drawn from vision. Is the same empirical strategy used in other sensory systems to contend with the same problem (i.e., the inability of animals to measure the actual properties of the world)? Based on accumulated anatomical, physiological, and psychophysical information, audition is the best bet in addressing this question in another modality. This chapter examines whether the perception of sound can also be explained empirically as a way to deal with a world in which the physical parameters of sound sources can’t be apprehended.

Evidence from Motion

Perceived motion is defined as the apparent speed and direction of objects that are translating and/or rotating in three-dimensional space. It has long been clear, however, that the perceived speeds and directions of moving objects disagree with physical measurements of motion. With respect to speed, the flash-lag effect has been a major focus; with respect to direction, the emphasis has been on the effects of apertures. These phenomena—and many others—raise the question of how we routinely succeed in the world despite blatant discrepancies between the motions we see and the physical speeds and directions of the objects we must deal with. Resolving this puzzle presents another body of evidence pertinent to whether empirical ranking is the way nervous systems link objective and subjective domains.

The Major Options

Given the argument and evidence that the operating principle of nervous systems is to generate neural associations on a wholly empirical basis, it makes sense to compare this framework with other ideas that neuroscientists have proposed for understanding brain function. These concepts fall into several broad categories: (1) neural operation based on detecting, computing, and representing stimulus features as such; (2) neural computation and representation based on statistical inferences about physical reality; and (3) neural operation based on efficient and/or predictive coding. Another concept pertinent to all these ideas, including neural operation as empirical association, is whether nervous systems are carrying out computations. This section reviews these conceptual options and some implications that follow.

Putting the Question in Perspective

Basic to the question of whether or not the brain and the rest of the human nervous system have a simple operating principle are some central facts about biology and its relation to neuroscience. What nervous systems do is best appreciated in the context of what all organisms must accomplish in order to survive and prosper, with or without neural assistance. Although the author’s understanding of these issues is no more than that of any other student who pays a modicum of attention to the broader sweep of scientific progress, this chapter considers some points of consensus. The aim is to situate the quest for a principle of neural function in the context of biology writ large.

Evidence from Lightness and Color

What, then, is the evidence that sensory systems link stimulus inputs to useful responses empirically as a means of generating successful behavior in a physical world that the senses cannot measure? This chapter focuses on evidence derived from studies of lightness and color in vision, the brain system that has been most extensively studied in this regard. The argument here, and in the following chapters that consider other perceptual qualities and systems, is that evolved circuitry based on accumulated experience with frequency of occurrence of biologically useful stimuli accomplishes this feat. This strategy, called empirical ranking theory, explains why the qualities we perceive are always at odds with physical measurements.

Evidence from Geometry

Dealing successfully with objects and conditions in the world entails another basic visual category: the geometry of objects. This domain is also rich in perceptual phenomenology that needs to be explained. The problem in understanding perceived geometry is much the same as the problem of understanding lightness values and colors: biological vision lacks the tools—in this case rulers, protractors, radar guns, laser range scanners—needed to measure geometrical reality. As a result, the geometries we see always differ from the measured parameters of the physical world. The aim of this chapter is to consider geometrical examples that further support the conclusion that vision operates by ranking perceptual values according to the frequency of occurrence of biologically useful stimulus patterns.