Crane brains and behavior 3 - Mental maps of local ecology in a Parahippocampal Place Area (PPA)?

For the past 18 days, our Sandhill Crane pair, Millie and Roy, have been trading incubation duties every 6-8 hours.  The off-duty crane feeds, loafs, calls, and inspects the neighborhood, including the nest-site pond and bogs across Goldstream Valley.

We believe that inspection allows cranes to monitor their environments. Inspection provides frequent updates to the mental map of the crane's world and also detects novelty (which might signal danger). In our previous Blogpost, we introduced the idea of such a map and drew parallels with spatial information that some bird species use to find food items that they have hidden previously.

Within the brain of a crane, where is the map of the neighborhood?  How is the information stored?

We can't readily investigate memory mechanisms by implanting electrodes into the brains of free-flying wild birds. But we can indirectly address questions about the mental capacities of wild birds by invoking laboratory research on people and other animal species.

For birds as for mammals, spatial data is stored in the hippocampus and associated parahippocampus, indicated by red arrows in the diagram of the bird brain¹.  In humans, the parahippocampal regions of the neocortex are implicated in spatial memory and navigation. The hippocampus is important for homing in pigeons² and caching of food items in many avian species^2,3. It is likely that the similarity in localized function reflects similarity by descent from their ancestral stem amniotes.  Fish also  store spatial information (including perhaps a cognitive map⁴) within their lateral pallium⁵, a brain region homologous to the hippocampus.

When Crows, Rooks, Jays, or Chickadees hide food tidbits for later retrieval, information about each item and its location is stored in the hippocampus.  The storage capacity is prodigious; tens of thousands of cached items are held in memory for later retrieval.  Items with limited "shelf life" (dead juicy caterpillars) are distinguished from durable items (acorns or peanuts)⁶.

Meticulous neuroanatomical research has shown that this region of a bird brain has an unusually regular architecture. The nerve cells are not randomly scattered but instead are clustered in patches or stripes that are reminiscent of the mammalian visual cortex⁷.

How is the data organized in the bird hippocampus?

At present, there are no data to directly answer this question in birds. For the present purposes, we'll look at on two of the many alternatives.

• Flat file - The mental map could be an analogue of a "flat file database" -- simply a list with environmental items in one field linked to responses in another field. This memory mechanism is analogous to the operant conditioning of experimental psychologists.  Pigeons in a Skinner box can distinguish among hundreds of geometric shapes and link each shape to a correct response.
  
  In the local ecology, a crane might compare each item in the environment with a previous environmental inventory.  Every object and its coordinates would be compared with memories to arrive at a response based in previous experience. An example of such a Flat File (like an Excel Spreadsheet) is shown in Footnote #8 below. 

The Flat File might recommend itself as a bird memory mechanism because it is scientifically reductionist. It is built from individually learned stimulus-response pairings - the classical learning paradigm that has been validated by many thousand pigeon pecks on keys in Skinner boxes.  It assumes no high-level cognition by the bird. This pairing of item and response must somehow be coupled with a mental mapping coordinate system that seems hard to build from the Skinner-box assumptions.

We suspect that from the perspective of a computer programmer, the flat file would be viewed as a robust and adequate memory mechanism. But it is a very clunky solution. 

The second alternative could stem from the architecture of the brain.

• Special Cognitive Center -  Parahippocampal Place Area (PPA). The crane's mental map could be homologous to a human mental map or "cortical representation of the local visual environment", to use the terminology of Nancy Kanwisher of the McGovern Institute for Brain Research at MIT⁹.
  
  In humans, Kanwisher's functional MRI (Magnetic Resonance Imaging) reveals the existence of the PPA and other localized specialized cortical centers for high-level cognitive functions (for example recognizing faces, places, or body parts)¹⁰.
  
  fMRI is a very powerful tool for mapping and imaging brain activity. If a group of nerve cells in an intact brain are working hard (firing often), they use lots of glucose and incur oxygen debt, just like your leg muscles when you run a 220-yard dash. The "wisdom of the body" dictates an increase in blood flow to bring more oxygen-rich hemoglobin to those oxygen-starved patches of cells. The ratio of fully loaded hemoglobin (rich in oxygen) to emptied hemoglobin (stripped of oxygen) can be precisely localized on the fMRI imaging screen.  When very tiny areas of the brain "light up", neuroscientists can link brain regions with cognitive tasks. 
  
  In humans, Kanwisher and her colleagues have shown that the human PPA (anatomically the "collateral sulcus adjacent to the parahippocampal cortex") lights up with fMRI in response to visual scenes.  It is particularly significant that for both people and rats, the PPA responds to the layout of the space, not simply to objects or landmarks. The objects must be mapped into a mental reference space, and recent work demonstrates that another class of nerve cells, called "grid cells", appear soon after birth in young rat pups^10,11. These grid cells can provide a coordinate system for locating each object specified by the place cells.
  
  As we discussed in a previous Blogpost, recent research has established the common origin (homology) of the hippocampal complex in birds with that of mammals, and numerous experiments have linked spatial memories with the bird hippocampus^3,4,6, apparently reflecting functional parallels with the mammalian hippocampus.
  
  Therefore we think it is reasonable to use the evolutionary, developmental, and functional identities between bird brains and mammal brains to propose that the bird hippocampus, like that of a mammal, may contain a PPA and grid cells. 

If cranes have a PPA that is homologous to mammals, then we suggest that the crane's PPA, a localized special cognitive center to recognize objects, could work in concert with grid cells to be the situs of environmental reference information.

We propose that maps in the crane PPA could accrue through experience and would be subject to updates and remodeling as the environment changes. Furthermore, they would provide a stable context to asses objects as they enter the visual field. Crane PPA mental maps could function at several scales, from the global scale as guides for seasonal migration to the local scale as a reference to register novelty. For Millie and Roy, that mental map might provide a reference picture which reveals novelty that augers threats.

As we enter the 21st new century, scientists are beginning to understand brain mechanisms that are linked to our human minds. Ignorance of the bird mind is even more profound.

Insightful research on human brains, like that from the Kanwisher laboratory¹², offers striking perspectives on brain function. There are intriguing parallels for the neuroscience underlying bird behavior. 
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1. Figure modified from Jarvis ED, Gunturkun O (25 colleagues), Reiner A, Butler AB, 2005. Avian brains and a new understanding of vertebrate brain evolution. Nature Reviews Neuroscience 6:151-159.
2. Kahn MC, Bingman VP, 2009. Avian hippocampal role in space and content memory. European J Neuroscience 30:1900-1908.
3. Clayton NS, 1998. Memory and the hippocampus in food-storing birds: a comparative approach. Neuropharmacol 37:441-452.
4. Jacobs LF. 2003. The evolution of the cognitive map. Brain Behav Evol 62:128-139.
5. Rodriguez F, Lopez JC, Vargas JP, Brogolio C, Gomez Y, Salas C, 2002. Spatial memory and hippocampal pallium through vertebrate evolution: Insight from reptiles and teleost fish. Brain Res Bull 57:499-503.
6. Emery NJ, Clayton NS, 2009. Comparative social cognition. Annu Rev Psychology 60:87-113.
7. Kovjanic D, Redies C, 2003. Small-scale pattern formation in a cortical area of the embryonic chicken telecephalon. J Compar. Neurology 456:95-104.
8. A crane might compare each item in the environment with a previous environmental inventory.

The mental item-and-response list could have fields, for example Stimulus-Object, Location, Compare-to-memory, Response that function like a name-and-address list.  In the Table below, we use arbitrary numbers for Location Coordinates. 

1. Stimulus (object seen in crane's vicinity)	2. Location Coordinates	3. Compare to Previously Stored Memory	4. Response
Spruce tree	1234, 4567	Spruce tree	Ignore
Poplar tree, leaves	1234, 4588	Poplar tree, no leaves	Update memory
Green grass on SE bank of pond	1234, 4592	Brown grass on SE bank of pond	Update memory
Red fox on SE bank	1234, 4592	New Item and a known Potential Predator	DANGER, attack
Birch tree, no leaves	1234, 4576	Birch tree, no leaves	Ignore
etc.	etc.	etc.	etc.

This Flat File database (an Excel Spreadsheet) can be built from a well-accepted learning paradigm in experimental psychology labs.   However, the explanatory table glosses over the "Coordinates"; perhaps this memory model also requires a series of fields to specify each location for each object, and therefore a much larger flat file. 

9. Epstein R, Kanwisher N, 1998. A cortical representation of the local visual environment Nature 392:598-601.
10. Wills TJ, Cacucci F, Burgess N, O'Keefe J, 2010 Development of the hippocampal cognitive map in preweaning rats. Science 328:1573-1576.
11. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser M-B, 2010 Development of the spatial representation system in the rat. Science 318: 1576-1580
12. Kanwisher N, 2010. Functional specificity in the human brain: A window into the functional architecture of the mind. Proc Nat Acad Sci USA (in press).