Exploration

Exploratory behaviors exist across all organisms. These behaviors enable the organism to learn and adapt to its surroundings. Exploration can be broadly classified as extrinsic and intrinsic exploration. While extrinsic exploratory behavior is associated with an external reinforcement, intrinsic exploratory behaviors tend to be independent of external reinforcements. Wood-Gush and Vestergaard (1989) further divided intrinsic exploration into inspective exploration that involves inspection of an object or surrounding, and inquisitive behaviors aimed at making a change rather than responding to change.

Exploratory behaviors may be the result of different motivations such as foraging in animals or simply curiosity as seen in a toddler exploring a novel object. Mc Reynolds (1962) suggests three possible classifications of exploratory behavior based on the type of motivation;

• Novelty-adjustive Behavior: These exploratory behaviors can be said to be aimed at minimizing or eliminating the novelness of a stimulus in order to elevate the ambiguity or anxiety associated with it. These behaviors can be attributed to situations wherein confrontation with novelty is not self-initiated.
• Novelty-seeking Behavior: These exploratory behaviors are often observed in situations where a choice or preference is involved. Unlike novelty-adjustive behaviors, novelty-seeking behaviors are catered by the organism’s own choice or curiosity for novelty.
• Goal-oriented Novelty-seeking Behavior: These novelty-exploring behaviors are encouraged by a reward rather than the novelty itself. An example of this behavior can be foraging by animals in a new environment.

Berlyne (1950) suggested that curiosity is the underlying motivation for exploratory behaviors. Exploratory behaviors are often considered markers of healthy development in infants and children. Bornstein, Hahn, and Suwalsky (2013) observed that active exploration during infancy has an observable impact on cognition and intelligence as the child develops. On the other hand, children with intellectual disabilities, such as those with Autism and Down Syndrome, exhibit differences in certain measures of explorative behaviors (Kawa, & Pisula, 2010). Exploratory motivations also provide insights into psychiatric disorders such as Schizophrenia (Siddiqui et al., 2018), neurodegenerative diseases such as Alzheimer’s disease (Daffner, Scinto, Weintraub, Guinessey, & Mesulam, 1992) and brain injury, among others.

Animal assays that involve assessment of explorative behaviors are popular in investigating anxiety and anxiety-related behaviors. In general, an animal’s inquisitive nature makes them explore novel surroundings or objects over familiar ones. However, exposure to extreme novelty can be detrimental to the animals. Another area of application is in learning and memory assessment. Since the recognition of novelty requires familiarization and learning of previously encountered contexts and stimuli, exploratory behaviors can provide insights into learning and memory impairments in different animal models.

2.1 Open Arena Assays

Open arenas are a popular design choice for exploratory behavior experiments. Animals, such as rodents, tend to have an averseness towards brightly lit open spaces and prefer closed dark spaces. The open arenas usually take advantage of this averseness to explore locomotion based exploratory behaviors of the animals, especially in anxiety and anxiety-related investigations. Most arena-based assays divide the space into invisible zones and observe the time spent in each zone.

Open Field

The Rodent Open Field test was developed by Hall and Ballachey (1932) and is used in a wide variety of tests involving exploratory behaviors. The apparatus consists of an open arena contained by high walls to prevent the animal from escaping the arena. The apparatus is available in different combinations of clear and opaque walls and the number of arenas in an apparatus to allow observation of multiple animals. Other variants include the Pig Open-Field Test.

3D Open Field

The 3D Open Field, unlike the traditional Open Field, is an elevated platform without any walls or safe spaces. The design, however, does include mesh slopes at two opposite edges of the open arena. The design is intended to create a conflict between the subject’s desire to explore a novel space and the fear that drives it to escape the open space.

Barnes Maze

The Barnes Maze is an elevated circular open arena with holes around the perimeter of the arena. The assay has a similar principle to the Morris Water Maze; the subject is required to explore the arena in order to find the hidden enclosed space placed under one of the holes. This apparatus involves elements of learning and memory that are encouraged by the subject’s escape/avoidance response to the open space. The apparatus is also available in different modifications such as the Radial Arm Barnes Maze.

Drosophila Shallow Chamber

The Drosophila Shallow Chamber was designed by Simon and Dickinson (Simon, & Dickinson, 2010) to create a shallow volume of space that allows the flies to move in a single layer. This design makes the observation of locomotion of flies easier to record and analyze.

2.2 Object Exploration Assays

Object recognition assays test the subject’s ability to differentiate between an already familiar cue and an unfamiliar cue. These tasks involve a certain degree of familiarization training and have a memory component involved, in particular, recognition memory. The tasks are also popular in assessing preference for exploring novel object over a familiar object. Exploratory behavior observation includes time spent exploring the object or in the vicinity of the object.

Novel Object Recognition

The apparatus is an open, square arena with high walls. The task may or may not require habituation to the apparatus. The general task usually involves familiarizing the subject with a single object following which the subject is tested in the test phase. In the testing phase, the previously familiarized object is placed along with a novel object, and the subject’s behavior is observed.

Novel Object Recognition Track Assay

The assay combines the advantages of the Delayed Non-Matching-to Sample (DNMS) task with the Novel Object Recognition task. The apparatus is a hexagonal shaped arena that is divided into seven equal-sized and 2 smaller compartments using dividers. The small compartments make the start and the end compartments of the track. The subjects are placed in the start compartment and are allowed to explore the track via one-way doors. Objects are placed in alternate chambers to create a delay between encounters.

Continuous Novel Object Recognition Assay

First described by Ameen-Ali, Eacott, and Easton (2012), the Continuous Novel Object Recognition Assay combines DNMS task and Spontaneous Object Recognition task. The apparatus is designed to minimize handling during test sessions and allows for complex tasks such as object-location and object-in-context, to be carried out. The apparatus consists of two E-shaped areas, one of which serves as the object area while the other serves as the holding area. The object area is rotatable to provide access to one of the four contexts in the apparatus. The two E-shaped areas are separated by opaque guillotine doors.

2.3 Olfactory Exploration Assays

Olfactory exploration behaviors often utilize a habituation-dishabituation protocol wherein the subject shows an increased time exploring the novel odor as opposed to familiar odor. In the animal kingdom, olfactory sensibility is crucial since many organisms rely on pheromones that are part of many interactions.

Hole Board

The Hole Board assay includes an Open Field arena with flooring that includes 4 or 16 holes. Under each hole, a small cylinder is placed which can be used to place stimuli. The Hole Board assay creates a rich testing environment that allows evaluation of a broad spectrum of exploratory and other behaviors in small animals.

Odor Span Test

The Odor Span Test was developed by Dudchenko, Wood, and Eichenbaum (2000) to evaluate odor recognition memory in rodents. The apparatus includes an elevated, large square arena with cups filled with scented sand (24 cups) placed around the boundary of the platform. The task can be used to observe odor based exploratory behavior as well as assessing odor-based recognition memory performances.

2.4 Goal-oriented Exploration Assays

Mazes are a popular choice for exploring goal-oriented novelty-seeking behaviors in animals. Mazes may involve the exploration of elaborate labyrinths or choice-based exploration. Observed data may include the number of times novelty was preferred, novel paths traversed, and time spent in the novel arm/zone.

T-Mazes

T-Mazes are a popular two-choice assay across a range of animal models. The apparatus design includes two choice arms perpendicular to a start arm. The simple set-up allows a controlled environment for observation of exploratory and goal-oriented novelty-seeking behaviors. Some of the T-Mazes available are the Rodent T-Maze, the Porcine T-maze, and the Zebrafish Bifurcating T-Maze. An adaptation of the T-Mazes are the Y-Mazes that share similar testing and design principle as the T-Mazes. However, unlike the perpendicular angle of the choice arms in the T-Mazes, the Y-maze choice arms are attached at a more natural angle of 120°. Some of the Y-Mazes available are the Rodent Y-maze, the Zebrafish Y-Maze, and the Bee Y-Maze.

Alley Maze

The Alley Maze was designed by Alley Maze was introduced by Uster, Bättig, and Nägeli (1976) as a probing environment without physiological rewards or punishment to study the exploratory behavior of rats. The maze is constructed using interconnected alleyways that give the apparatus an overall hexagonal shape. The alleyways can be configured as desired to introduce novel pathways into the tasks.

Radial Arm Maze

The Radial Arm Maze (RAM) is yet another popular choice-based exploratory assay. The apparatus consists of multiple-choice arms radiating from a central platform or arena. The multiple-choice arms allow the creation of different novel configurations that allow observation of novelty-seeking explorations. Some of the Radial Arm Mazes available include the Pig 8-arm RAM and the Rodent 8-arm RAM.

Elevated Asymmetrical Plus Maze

The Elevated Asymmetric Plus maze was first described by Ruarte, Orofino, and Alvarez in the 1997 paper aimed at assessing conflictive exploration. The apparatus consists of arms that have a combination of walled and unwalled choice alleys that pit the rodent’s explorative inquisitiveness against its fear of open spaces or falling.

Labyrinth

The Labyrinth is a fully automated maze that allows a range of protocols and configurations to be applied. The flexible apparatus can be used to test a range of exploratory behaviors and exploratory motivations.  

2.5 Forced Explorative Assays

Forced explorative assays usually test novelty-adjustive behaviors. More often, than not, these tasks involve incentives to motivate the subjects to complete the task. Observed behaviors may include the willingness to explore the apparatus and perform the task and level of anxiety expressed by the subject.

Morris Water Maze

The Morris Water Maze (MWM) was developed by Richard G. Morris in 1981. In addition to being an open arena, it also includes the aversive element, water. The task usually involves exploring the pool of water in order to find the escape platform by the subject. In comparison to other types of open arenas, the Morris Water Maze tends to be relatively more stressful for the subject. The apparatus allows different modifications such as MWM Open Field Tower and maze inserts allow different investigatory protocols to be applied.

Mammalian Diving Response

The Mammalian Diving Response assay involves a hairpin maze pool and is usually used in the assessment of diving reflex in animals. The task usually involves swim training without the cover of the maze to familiarize the subject with the maze. Following the habituation, the maze is covered so that the subject is forced to dive and explore the maze in order to find the escape platform.

Exploratory behaviors form an important part of development in children. In young children, exploratory behaviors are often seen in the form of play. Familiarization and exploring the environments and other stimuli allow children to develop cognitive skills and knowledge. Diminished or changed exploratory behaviors may provide insights into developmental delays or disorders. Object exploration and spatial exploration tests are often used to score exploratory behaviors in children taking into account the variability of exploration patterns, the affordance of stimuli, integration of multimodal information and attentiveness, combinatorial aspects of stimuli, as well as atypical exploratory behaviors (Hellendoorn et al., 2015).

Tests such as the Novelty Exploration Task (Siddiqui et al., 2018) where participants are observed, and scored, exploring a novel environment containing familiar and unfamiliar objects allow investigation of motivation deficits associated with different disorders and diseases. Novelty-seeking behaviors characterized by impulsive, exploratory, or sensation-seeking behavior often accompany psychiatric disorders such as drug (Ersche, Turton, Pradhan, Bullmore, & Robbins, 2010) and alcohol addictions (Noel et al., 2011). Investigation of these behaviors allows expansion of the understanding of the impact on an individual’s cognitive capacity and memory abilities.

While a majority of human-based research revolves around observing and scoring (sometimes self-assessment) behaviors (For digital healthcare tools, visit Qolty) in controlled, real-world environments, technological advancements in the field of virtual reality have opened up new dimensions of exploratory behavior investigations (For virtual reality tools visit Simian Labs). Primarily, the rich environments that can be created to closely mimic, natural real-world interactions and situations make virtual reality an efficient tool of assessment. Apart from the assessment of exploratory behaviors, virtual reality also provides the opportunity to explore and develop tools to allow differently-abled individuals, such as the blind (Picinali, Afonso, Denis, & Katz, 2014), to explore their surroundings. (For human virtual reality experiments, click here)

The following are a few suggestions to perform experiments in an ethical manner,

• Animals should be habituated to handling to minimize the effects of handling stress.
• When introducing novelty, it isn’t overwhelming for the subject. Overwhelmed subjects may not display expected explorative behaviors.
• Appropriate lighting should be used to illuminate the apparatus since some animals may display a strong aversion to bright lights.
• Animal testing following injury or other pain-inducing treatment should ensure that pain is minimized to an acceptable level for the research.
• Cushion floor or other measures should be taken in a task that involves falls to prevent injury to the animals.
• Following experiments that involve swimming, subjects must be thoroughly dried and kept in warm environments.
• Overtraining of the animals can result in decreased motivation to perform the task and muscle fatigue. Hence, appropriate rest intervals or task durations should be maintained.

Apart from the above guidelines, efforts should be made to ensure the overall wellbeing of the animals in the laboratory. Animals should not be subjected to unnecessary stress or mishandling at any time.

Further to gain the most from the experiments, apparatuses should be cleaned as necessary to prevent any lingering olfactory cue from influencing the subject behavior. It is advisable to use an automated tracking and recording system such as the Noldus EthoVision XT to assist with the observation of behaviors.

In human experiments and research, the following are a few guidelines that should be followed

• Explicit consent of the participants should be obtained prior to testing.
• Experiments should be age-appropriate and take into consideration all medical factors.
• Safety and well-being of the participants should be prioritized above all.
• Experiments that involve potential triggering set-ups should be carefully created so as not to overwhelm or stress the participant.
• Appropriate measures should be taken when using virtual reality for experimentation.

Familiarization and developing an understanding of the environment and the various stimuli present in it contributes to the survivability of the organism. Exploration, whether motivated by rewards, goal, or curiosity, is a crucial aspect of development across all organisms. Exploratory behaviors evolve with age as well as experience and decrease as novelty turns into familiarity. As such exploratory behaviors are also dependent on the physical as well as cognitive abilities of an individual. Thus, investigation of exploratory behaviors and the motivations behind them can help understand different disorders and diseases, and develop effective treatments.

Animal behavioral studies often employ exploration-based assays in assessments involving drug-testing, anxiety, and goal-oriented behaviors. The types of assessments can vary depending on the complexity of the apparatus and the type of stimuli used. Researchers now can be seen taking advantage of virtual reality to translate animal assays into human applications such as the Virtual Morris Water Maze and the Virtual Radial Arm Maze. As opposed to the real-world controlled environments that may not always mimic real situations and interactions, the use of virtual reality allows testing in rich environments that can easily be tailored and controlled by the investigator.

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