Obituary for Professor Richard J. Andrew, 1932–2018

 

Richard J. Andrew, Emeritus Professor of Biology, died on 15 August 2018 aged 86. He was a pioneer and very prominent figure in research on animal behaviour and associated brain mechanisms. In a scientific career spanning almost six decades, lateralization of brain and behaviour became his principal area of research over the last four decades of his life.

Son of Janet and Bruce Andrew, deputy head of Chesterfield Grammar School, Derbyshire, UK, Richard attended that school, became Head Boy and went to Cambridge University when he was only 17 years old. At Cambridge University, he studied Zoology followed by a PhD on buntings supervised by Robert Hinde at the Madingley Field Station (papers published in the 1950s, e.g., Andrew, 1957). After finishing university, he was called-up for National Service, which in his case was learning Russian and becoming an interpreter. He then went to the Edward Grey Institute in Oxford of Field Ornithology (EGI) as a post-doctoral student in 1958, where he studied mechanisms involved in the mobbing behaviour of blackbirds and their vocalizations (see Anderson, 2013, Figure 15). This research led to a series of papers on “the motivational organisation controlling mobbing calls in the blackbird” published in Behaviour (e.g., Andrew, 1961a, 1961b, 1961c).

In 1959 Richard was appointed as an Assistant Professor at Yale University, where he studied vocal and facial communication in non-human primates. He was very much a leader in this field and wrote some important, widely quoted papers (Andrew, 1963a, 1963b). He conceived the idea that primate facial expressions are a secondary consequence of the vocalizations produced when in an emotional state (Andrew, 1963b, 1964a, 1965, 1976). He was also interested in vocal mimicry and published a paper in Science relating evolution of intelligence to vocal mimicking (Andrew, 1962), a topic that has more recently received considerable attention and continues to do so. Also, when at Yale, he began research on precocious adult behaviour in newly hatched domestic chicks. In so doing, he devised a “hand-thrust test” to measure juvenile copulation, later used by a number of researchers together with to a similar method developed by Richard for scoring aggressive behaviour in chicks by using a moving hand to elicit visual tracking and attack responses (Andrew, 1966a). At that time Richard investigated the role of testosterone in causing precocious adult behaviour (Andrew, 1966a) and the relationship between following an imprinting stimulus and precocious adult behaviour (Andrew, 1964b, 1966b).

In 1965 he was recruited to a Readership at Sussex University by the founding Dean of the School of Biological Sciences, John Maynard Smith, for his innovated work animal behaviour, as an early leader in what was to become Cognitive Science, bringing together talent and ideas in the disciplines of ethology, psychology, philosophy, neuroscience and artificial intelligence. At Sussex University Richard joined others in this emerging field, including Stuart Sutherland, Christopher Longuet-Higgins and Aaron Sloman. At Sussex University, Richard established a group that was unique in the UK for combining the ethological study of behaviour with neurophysiology, launching in 1972 the first neurobiology degree in the UK.

In 1968 Richard was promoted to a Chair and he remained at Sussex University for the rest of his academic life. His broader contributions included a period as Dean of Biology and another as President of the Association of the Study of Animal Behaviour. His main research during the early years of his appointment at Sussex University was on behaviour and brain mechanisms in chicks. He investigated, among others topics, the diencephalic regions that, when stimulated, can elicit escape responses (Andrew & Oades, 1973), thereby demonstrating similarities between the neural control of the escape-hide-freeze system in birds and mammals and pointing to the possibility that this system is of ancient origin. He was also able to show that electrical stimulation of the diencephalon of conscious chicks caused them to produce a number of characteristic calls, including startle calls and peeps associated with scanning movements of the head (Andrew, 1973).

Another important interest at that time was in how testosterone leads chicks to become behaviourally persistent, particularly during food searching behaviour (Andrew, 1972). This work was done with his then Ph.D. student Lesley Rogers, and it began a lifelong collaboration. They found that, when given a choice of pecking at red or yellow grains scattered on a background of pebbles, chicks treated with testosterone searched persistently for grains of one colour, whereas untreated chicks pecked with short runs on one colour and then the other (Andrew & Rogers, 1972). Testosterone-treated chicks were also shown to be less attentive to stimuli entering their lateral field of vision than were untreated chicks (Rogers & Andrew, 1989). The effect of steroid sex hormones on behaviour, attention, and also on memory formation, was studied in more detail by Richard (Andrew, 1983a; Clifton & Andrew, 1989).

After lateralization of function in the chick brain had been discovered by Rogers in the 1970s (Rogers & Anson, 1979), Richard turned his interest to the study of lateralization of behaviour. This was the topic that dominated the last part of his career.

The procedure used by Rogers, then at the Australian National University, to discover lateralization in the chick was a logical follow on for her work on inhibitors of memory formation, using the chick as a model. It involved injecting cycloheximide into one hemisphere, or the other, and then testing different patterns of behaviour after a period of delay (Rogers, 1980, 1982): treatment of the left hemisphere caused long-lasting impairment the chick’s ability to learn to discriminate grain from a background of small pebbles, whereas the same treatment of the right hemisphere had no effect on this behaviour (Rogers & Anson, 1979). Administration of cycloheximide to either the left or right hemisphere also revealed lateralized control of attack and copulation responses (Rogers, 1982). The latter functions are controlled by the right hemisphere, whereas they are suppressed when the left hemisphere is being used.

Richard took the next step in this line of research by devising a very simple way of revealing lateralization of behaviour; by covering one or the other eye of the chick and so comparing behaviour controlled by use of the left versus right eye system (Andrew, 1983b; Andrew, Mench, & Rainey, 1982; Mench & Andrew, 1986). Since each eye sends its input to the contralateral forebrain hemisphere, monocular testing is a way of showing lateralization, not only in chicks but in a wide range of species, especially in those with their eyes positioned laterally, and hence with large monocular visual fields (Rogers & Andrew, 2002). The insight that led Richard to use monocular testing to reveal lateralization could also be applied to testing and observing animals in their natural habitats, and a number of papers have reported lateralized eye use in wild populations of birds (e.g., in stilts, Ventolini et al., 2005; in Australian magpies, Koboroff, Kaplan, & Rogers, 2008) and other species. In fact, many papers reporting differential responding by the left and right eye have been published over the last four decades (reviewed in Rogers, Vallortigara, & Andrew, 2013) and monocular testing continues to be a most valuable technique.

Using monocular testing, Richard studied developmental changes in lateralized fear behaviour over the first two weeks of the chick’s life post-hatching and discovered sharp changes in fear responses at particular ages: monocular tests showed that the left hemisphere was in control during the first week of life and then a major transition to control by the right hemisphere occurs between days 9 and 10. Notably, it is at this age that chicks tested binocularly display elevated levels of fear (Andrew & Brennan, 1983). Later, with his student Lance Workman, he drew attention to changes in general behaviour chicks that coincide with transitions between left and right hemisphere control. For example, it is on day 10, when the left eye and right hemisphere assume control and attention shifts to spatial cues, that chicks first begin to move independently of the hen (Andrew, 1988; Workman & Andrew, 1989). Then, with another student, Meena Dharmaretnam, Richard scored preferred eye for viewing stimuli at different ages: they found preferred use of the right eye (left hemisphere) to view a hen at most ages during the first week after hatching, especially on day 8, followed by a shift to a left eye (right hemisphere) preference on days 10 and 11 post-hatching (Dharmaretnam & Andrew, 1994). These shifts in hemisphere use fitted the previously shown pattern of left hemisphere susceptibility to cycloheximide’s effect on learning ability up to day 8 followed by right hemisphere susceptibility on days 10 and 11 (Rogers, 1991). Richard noted similar age-dependent shifts in hemisphere use in human infants (Andrew & Dharmaretnam, 1991; Dharmaretnam & Andrew, 1994; MacKenzie, Andrew, & Jones, 1998; and see also Regolin & Vallortigara, 1996).

In fact, Richard hypothesized that brain lateralization was present in the very first vertebrate species (Andrew, 2002a); namely, in the ancestral chordates, which had extreme body asymmetry, especially of the mouth position and the associated neural connections. These asymmetries, he reasoned, were the beginning of the left hemisphere’s specialization for control of feeding, which included search for inanimate food, such as grains, or in pursuit of live prey. Asymmetries in these first vertebrates were, Richard hypothesized, the basis of asymmetries extant in all present-day vertebrates, including humans (discussed in Chapter 3 of Rogers et al., 2013).

In collaboration with Giorgio Vallortigara, Richard investigated lateralization of chicks’ abilities to detect changes in response to an imprinted stimulus. They found that chicks using their left eye respond to small changes in the imprinted stimulus, whereas those using their right eye respond only to larger changes in the stimulus (Vallortigara & Andrew, 1991). This lateralized difference, they went on to show, means that chicks can recognize familiar from unfamiliar chicks when they can use their left eye (and right hemisphere) but not when they are forced to use only their right eye (and left hemisphere) (Vallortigara & Andrew, 1994a). It was the first evidence for the role of the right hemisphere in social behaviour, recently shown to be characteristic of a wide range of vertebrate species (Karenina, Giljov, Ingram, Rowntree, & Malashichev, 2017).

Research collaboration with Giorgio Vallortigara also led to the discovery of lateralized responding to olfactory stimuli in chicks (Vallortigara & Andrew, 1994b), achieved by occluding the left or right nostril of the chick and then testing memory of an odour. This demonstrated that lateralization in the chick is not limited to the visual modality. Furthermore, Richard and co-workers were able to show lateralization of auditory processing in chicks (Miklósi, Andrew, & Dharmaretnam, 1996, and summarized in Andrew & Watkins, 2002).

Several years later, Richard pursued the lateralized role of memory formation in the chick using the passive avoidance learning task (PAL), in which the chick is presented with a coloured bead at which it can peck, thus receiving a bitter taste of methyl anthranilate, with which the bead had been coated. Extensive research on the biological basis of memory formation had been conducted using this test in Steven Rose’s group at the Open University and in Marie Gibbs’ group at La Trobe University (for a summary see Rose, 1992, and Gibbs, 2016). Also, the lateralized location of the memory in the hemispheres had been reported by Rose and colleagues. Richard hypothesized that the predominant role of the left hemisphere in PAL is due to that hemisphere’s role in control of manipulation and motor responses including use of the beak (Andrew, Tommasi, & Ford, 2000), also evident, as he and Luca Tommasi were able to demonstrate, as preferred left-eye use by chicks as they approach bowl of food covered by a lid and thus requiring manipulation using the beak in order to gain access to the food (Andrew et al., 2000). This contrasts to the role of the right hemisphere in spatial tasks, first suggested by Richard in his 1982 paper (Andrew et al., 1982).

Using PAL and various pharmacological agents to inhibit memory formation, Richard discovered separate time courses of memory traces in the left and right sides of the brain (Andrew, 1997, 1999). Successful encoding of memory of PAL depends on interactions between these two differently timed processes in the hemispheres. PAL was also studied using monocular testing and this revealed enhanced recall 25 min after training when the left eye was in use, and at 30–32 min after training when the right eye was in use (Andrew, 2002b; Andrew & Brennan, 1985). These results led to ideas and discussion about hemispheric differences in timing of short-, immediate- and long-term memory processes and the coinciding periods of interaction between the hemispheres during memory formation (Andrew, 1985). Richard then presented evidence brief events when retrieval is unusually good recur cyclically and according to cycles with different timing in the left and right hemispheres (Andrew, 1991a).

A role of testosterone in enhancing PAL learning in the chick was also found by Richard, working with Peter Clifton in his laboratory and Marie Gibbs at La Trobe University (Andrew, Clifton, & Gibbs, 1981). Following on from this, Richard reported experiments showing sex differences in age-related fear behaviour and related these to differences in interhemispheric interactions (Andrew & Brennan, 1984).

Richard was always conscious of the possibility that these studies could enhance understanding of hemispheric specializations in humans. For example, a conclusion to a paper by Rashid and Andrew (1989) states,

Both the different specialization of the two eye systems of the chick and the way in which they may collaborate by concentrating on different aspects of the task … offer interesting models for comparison with the very wide range of theories concerning human hemisphere interaction.

One of the special aspects of lateralization of visual behaviour in the chick is its dependence on light exposure of the eggs/embryos just before hatching. This role of light experience, discovered by Rogers (1982), is a consequence of the turned position of the of the embryo in the egg, allowing only the right eye to be stimulated by light passing through the shell and membranes at this critical stage of development. This was demonstrated by finding an absence of visual asymmetry in chicks hatched from eggs incubated in the dark (Rogers, 1982) and later by reorienting the embryo before hatching so that the left eye only received stimulation by light, thereby reversing the direction of lateralization (Rogers,1990). During a visit to the University of New England, Richard and Lesley Rogers worked together and were able to advance understanding of the role of light in establishing specific asymmetries of visual behaviour (Rogers, Andrew, & Johnston, 2007) and to demonstrate that the light exposure has no cross-modality effect on the development of olfactory lateralization (Rogers, Andrew, & Burne, 1998) or on lateralization of choice to approach a visual stimulus on which the chicks had been imprinted (Andrew, Johnston, Robins, & Rogers, 2004).

Richard organized a conference on using the chick as a model to investigate learning, memory and development, held in 1988 at Sussex University and leading to volume edited by Richard and published by Oxford University Press (Andrew, 1991b). This book became a valuable source of information and ideas for laboratories conducting research on chicks.

From the late 1990s on, Richard and colleagues began to study lateralized behaviour using the zebrafish as a model species (Miklósi & Andrew, 2006; Miklósi, Andrew, & Savage, 1997), chosen partly because this species might shed more light on his hypothesis about the evolution of brain lateralization and the role of the habenular nuclei (Andrew, 2009) and because it allowed experimentation of lateralization in genetic mutants (Barth et al., 2005), as well as easy access to test behaviour in the larval stages of development (which was studied with respect to lateralization with Valeria Sovrano; Sovrano & Andrew, 2006). Firstly, the research group showed similarities between lateralization in zebrafish larvae and chicks; viz., use of the left eye to view a familiar stimulus (e.g., a partner) and sustained use of the right eye when a decision must be made before responding (Miklósi et al., 1997). As an example of the latter, zebrafish use the right eye when they view a small bead before deciding to bite it (Miklósi & Andrew, 1999). The conclusion of the latter paper stated that a basic pattern of lateralization is “consistent throughout the vertebrates”. That pattern is: use of the left hemisphere when fleeing or attack must be inhibited while a decision about responding must be made, and use of the right hemisphere for “free performance of such responses (fleeing or attack) with minimal latency” when required. This pattern has been studied in detail in the chick (Andrew & Rogers, 2002).

Concerning development of lateralization, and in collaboration with Daniel Osorio, Adam Miklósi, Sergey Budaev and others, he showed that that light also influences the development of lateralization in the zebrafish, as it does so in the chick but at a different stage of development and via a different neural mechanism (Andrew et al., 2009; Andrew, Osorio, & Budaev, 2009; Budaev & Andrew, 2009).

Asymmetry in the zebrafish mutant strain fsi (frequent-situs-inversus) is reversed at both the visceral and anatomical levels. Behavioural testing of these mutant fish revealed that their behaviour was reversed in only some responses: that is, it was not simply a total reversal of behaviour in keeping with the reversed viscera and neuroanatomy. As Richard was instrumental in showing, this partial reversal of behaviour in fsi fry generated a new behavioural phenotype, evident in the response to novel stimuli. In other words, an entirely new spectrum of behaviour had emerged in individuals with reversed structural asymmetry (Barth et al., 2005). This novel finding was an advance in the field with implications for understanding situs inversus in humans. Although it was the study of behavioural lateralization in the zebrafish that captured Richard’s attention and became the focus of his research in his later years, he never left behind comparisons with lateralization in other species, chicks especially.

Also, in the 2000s, following collaboration with Giorgio Vallortigara and his younger colleagues—Lucia Regolin and Luca Tommasi (both of whom also spent time as post-doctoral students in Richard’s laboratory), Richard visited Italy several times, and also returned to his early interests on brain work, taking part in experiments on spatial learning and its lateralization in the chicks’ hippocampal formation (Tommasi, Gagliardo, Andrew, & Vallortigara, 2003).

We have not mentioned or cited all of Richard’s publications in this short acknowledgement of his important contribution to the study of animal behaviour and neuroethology. One of his more recent publications (Andrew, 2009) considered the evolution of brain and behavioural asymmetry from left-right differences in habenulae of early tetrapods and, as well, discussed asymmetry in invertebrate species, the latter having by then been found in bees (Rogers & Vallortigara, 2008). In vertebrates he saw a common pattern of right eye use in sustained pursuit (as in catching prey) and left eye use to attend to valent stimuli and to promote intense response (as in escape response), later in evolution to be expressed as strong emotion (see MacNeilage, Rogers, & Vallortigara, 2009; Vallortigara & Versace, 2017).

Richard was an original thinker, always with stimulating and fascinating ideas. Citation of even his earlier research continued throughout his entire career. An absolutely dedicated and inspired scientist, he continued to write and publish until the last few months of his life.

In addition to his focus on science, Richard had a wide range of interests in the humanities and politics. One of us (GV) has a clear and somewhat embarrassing memory of visits to ancient Italian’s towns, with Richard showing more prompt translations of Latin epigraphs from columns and the ruins of buildings than Giorgio. He similarly surprised others by mentioning or reading Catullo or Russian poets during conversations in his garden in Lewes, sometimes cajoled lovingly by his wife, Diana.

His students and colleagues remember his group as relaxed and friendly, and of morning tea meetings in which ideas were discussed and shared in ways that enlivened their research. Richard will always be respected and sorely missed by his students, academic colleagues and his family, especially by his wife Diana Andrew, who gave him strong and invaluable support throughout his career. Richard’s lasting influence stems not only from his outstanding research but from friendships with former students and colleagues in ethology and neuroscience.

Correction Statement

This article has been republished with minor changes. These changes do not impact the academic content of the article.